Diabetes and Exposure to Environmental Lead (Pb)
Abstract
:1. Introduction
2. Human Lead Exposure Patterns
3. Evidence that Lead Exposure is Pro-diabetic
3.1. Association of Lead and Other Metals with Metabolic Disorders
3.2. Rodent Studies
3.3. Epigenetic Effects of Lead Exposure
4. Molecular Mechanisms by Which Lead Might Promote Diabetes
4.1. Lead Causes Oxidative Stress, a Risk Factor for Diabetes
4.2. Lead Alters Intracellular Signaling Pathways
4.2.1. Lead Increases Resting Intracellular Ca++
4.2.2. Lead Modulates PKC Activity
4.2.3. A Potential Link Between Lead and Rev-erb-α
5. Conclusions/Future Prospects
Author Contributions
Funding
Conflicts of Interest
References
- Song, Y.; Chou, E.L.; Baecker, A.; You, N.C.Y.; Song, Y.; Sun, Q.; Liu, S. Endocrine-disrupting chemicals, risk of type 2 diabetes, and diabetes-related metabolic traits: A systematic review and meta-analysis. J. Diabetes 2016, 8, 516–532. [Google Scholar] [CrossRef] [PubMed]
- Calafat, A.M.; Kuklenyik, Z.; Reidy, J.A.; Caudill, S.P.; Ekong, J.; Needham, L.L. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ. Health Perspect. 2005, 113, 391–395. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.W.; Yang, C.Y.; Huang, C.F.; Hung, D.Z.; Leung, Y.M.; Liu, S.H. Heavy metals, islet function and diabetes development. Islets 2009, 1, 169–176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cave, M.; Appana, S.; Patel, M.; Falkner, K.C.; McClain, C.J.; Brock, G. Polychlorinated biphenyls, lead, and mercury are associated with liver disease in American adults: NHANES 2003–2004. Environ. Health Perspect. 2010, 118, 1735–1742. [Google Scholar] [CrossRef] [PubMed]
- Zhai, H.; Chen, C.; Wang, N.; Chen, Y.; Nie, X.; Han, B.; Li, Q.; Xia, F.; Lu, Y. Blood lead level is associated with non-alcoholic fatty liver disease in the Yangtze River Delta region of China in the context of rapid urbanization. Environ. Health 2017, 16, 93. [Google Scholar] [CrossRef] [PubMed]
- Afridi, H.I.; Kazi, T.G.; Kazi, N.; Jamali, M.K.; Arain, M.B.; Jalbani, N.; Baig, J.A.; Sarfraz, R.A. Evaluation of status of toxic metals in biological samples of diabetes mellitus patients. Diabetes Res. Clin. Pract. 2008, 80, 280–288. [Google Scholar] [CrossRef] [PubMed]
- Padilla, M.A.; Elobeid, M.; Ruden, D.M.; Allison, D.B. An Examination of the Association of Selected Toxic Metals with Total and Central Obesity Indices: NHANES 99–02. Int. J. Environ. Res. Public Health 2010, 7, 3332–3347. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.-J.; Wang, S.-L.; Chiou, J.-M.; Tseng, C.-H.; Chiou, H.-Y.; Hsueh, Y.-M.; Chen, S.-Y.; Wu, M.-M.; Lai, M.-S. Arsenic and diabetes and hypertension in human populations: A review. Toxicol. Appl. Pharmacol. 2007, 222, 298–304. [Google Scholar] [CrossRef] [PubMed]
- Moon, S.-S. Association of lead, mercury and cadmium with diabetes in the Korean population: The Korea National Health and Nutrition Examination Survey (KNHANES) 2009–2010. Diabet Med. 2013, 30, e143–e148. [Google Scholar] [CrossRef] [PubMed]
- Bener, A.; Obineche, E.; Gillett, M.; Pasha, M.A.; Bishawi, B. Association between blood levels of lead, blood pressure and risk of diabetes and heart disease in workers. Int. Arch. Occup. Environ. Health 2001, 74, 375–378. [Google Scholar] [CrossRef] [PubMed]
- Kolachi, N.F.; Kazi, T.G.; Afridi, H.I.; Kazi, N.; Khan, S.; Kandhro, G.A.; Shah, A.Q.; Baig, J.A.; Wadhwa, S.K.; Shah, F.; et al. Status of toxic metals in biological samples of diabetic mothers and their neonates. Biol. Trace Elem. Res. 2011, 143, 196–212. [Google Scholar] [CrossRef] [PubMed]
- Hanna-Attisha, M.; LaChance, J.; Sadler, R.C.; Champney Schnepp, A. Elevated Blood Lead Levels in Children Associated With the Flint Drinking Water Crisis: A Spatial Analysis of Risk and Public Health Response. Am. J. Public Health 2015, 106, e1–e8. [Google Scholar] [CrossRef] [PubMed]
- Searle, A.K.; Baghurst, P.A.; van Hooff, M.; Sawyer, M.G.; Sim, M.R.; Galletly, C.; Clark, L.S.; McFarlane, A.C. Tracing the long-term legacy of childhood lead exposure: A review of three decades of the port Pirie cohort study. Neurotoxicology 2014, 43, 46–56. [Google Scholar] [CrossRef] [PubMed]
- Ris, M.D.; Dietrich, K.N.; Succop, P.A.; Berger, O.G.; Bornschein, R.L. Early exposure to lead and neuropsychological outcome in adolescence. J. Int. Neuropsychol. Soc. 2004, 10, 261–270. [Google Scholar] [CrossRef] [PubMed]
- Surkan, P.J.; Zhang, A.; Trachtenberg, F.; Daniel, D.B.; McKinlay, S.; Bellinger, D.C. Neuropsychological function in children with blood lead levels <10 micro g/dL. Neurotoxicology 2007, 28, 1170–1177. [Google Scholar] [PubMed]
- Joshu, C.E.; Boehmer, T.K.; Brownson, R.C.; Ewing, R. Personal, neighbourhood and urban factors associated with obesity in the United States. J. Epidemiol. Commun. Health 2008, 62, 202–208. [Google Scholar] [CrossRef] [PubMed]
- Centers for Disease Control and Prevention (CDC) Blood lead levels—United States, 1999–2002. MMWR Morb. Mortal. Wkly. Rep. 2005, 54, 513–516.
- Raymond, J.; Brown, M.J. Childhood Blood Lead Levels in Children Aged < 5 Years—United States, 2009–2014. MMWR Surveill. Summ. 2017, 66, 1–10. [Google Scholar] [PubMed]
- Centers for Disease Control and Prevention, Childhood Lead Poisoning Data, Statistics, and Surveillance. Available online: https://www.cdc.gov/nceh/lead/data/index.htm (accessed on 1 July 2018).
- Patterson, C.C.; Shirahata, H.; Ericson, J.E. Lead in ancient human bones and its relevance to historical developments of social problems with lead. Sci. Total Environ. 1987, 61, 167–200. [Google Scholar] [CrossRef]
- Michigan Department of Health & Human Services. Michigan’s Childhood Lead Poisoning Prevention Program, Data and Research. Available online: https://www.michigan.gov/lead/0,5417,7-310-66221_66223---,00.html (accessed on 10 March 2018).
- Jones, O.A.; Maguire, M.L.; Griffin, J.L. Environmental pollution and diabetes: A neglected association. Lancet 2008, 371, 287–288. [Google Scholar] [CrossRef]
- Targher, G.; Bertolini, L.; Padovani, R.; Rodella, S.; Tessari, R.; Zenari, L.; Day, C.; Arcaro, G. Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients. Diabetes Care 2007, 30, 1212–1218. [Google Scholar] [CrossRef] [PubMed]
- Williamson, R.M.; Price, J.F.; Glancy, S.; Perry, E.; Nee, L.D.; Hayes, P.C.; Frier, B.M.; Van Look, L.A.F.; Johnston, G.I.; Reynolds, R.M.; et al. Edinburgh Type 2 Diabetes Study Investigators Prevalence of and risk factors for hepatic steatosis and nonalcoholic Fatty liver disease in people with type 2 diabetes: The Edinburgh Type 2 Diabetes Study. Diabetes Care 2011, 34, 1139–1144. [Google Scholar] [CrossRef] [PubMed]
- Weaver, V.M.; Ellis, L.R.; Lee, B.-K.; Todd, A.C.; Shi, W.; Ahn, K.-D.; Schwartz, B.S. Associations between patella lead and blood pressure in lead workers. Am. J. Ind. Med. 2008, 51, 336–343. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weaver, V.M.; Lee, B.-K.; Ahn, K.-D.; Lee, G.-S.; Todd, A.C.; Stewart, W.F.; Wen, J.; Simon, D.J.; Parsons, P.J.; Schwartz, B.S. Associations of lead biomarkers with renal function in Korean lead workers. Occup. Environ. Med. 2003, 60, 551–562. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weaver, V.M.; Lee, B.-K.; Todd, A.C.; Jaar, B.G.; Ahn, K.-D.; Wen, J.; Shi, W.; Parsons, P.J.; Schwartz, B.S. Associations of patella lead and other lead biomarkers with renal function in lead workers. J. Occup. Environ. Med. 2005, 47, 235–243. [Google Scholar] [CrossRef] [PubMed]
- Weaver, V.M.; Griswold, M.; Todd, A.C.; Jaar, B.G.; Ahn, K.-D.; Thompson, C.B.; Lee, B.-K. Longitudinal associations between lead dose and renal function in lead workers. Environ. Res. 2009, 109, 101–107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsaih, S.; Korrick, S.; Schwartz, J.; Amarasiriwardena, C.; Aro, A.; Sparrow, D.; Hu, H. Lead, diabetes, hypertension, and renal function: The normative aging study. Environ. Health Perspect. 2004, 112, 1178–1182. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fadrowski, J.; Navas-Acien, A.; Tellez-Plaza, M.; Guallar, E.; Weaver, V.; Furth, S. Blood lead level and kidney function in US adolescents: The Third National Health and Nutrition Examination Survey. Arch. Intern. Med. 2010, 170, 75–82. [Google Scholar] [CrossRef] [PubMed]
- Singhal, R.; Kacew, S.; Sutherland, D.; Telli, A. Plumbism: Adaptive changes in hepatic and renal metabolism. Res. Commun. Chem. Pathol. Pharmacol. 1973, 6, 951–962. [Google Scholar] [PubMed]
- Stevenson, A.; Merali, Z.; Kacew, S.; Singhal, R. Effects of subacute and chronic lead treatment on glucose homeostasis and renal cyclic AMP metabolism in rats. Toxicology 1976, 6, 265–275. [Google Scholar] [CrossRef]
- Whittle, E.; Singhal, R.; Collins, M.; Hrdina, P. Effects of subacute low level lead exposure on glucose homeostasis. Res. Commun. Chem. Pathol. Pharmacol. 1983, 40, 141–154. [Google Scholar] [PubMed]
- Mostafalou, S.; Baeeri, M.; Bahadar, H.; Soltany-Rezaee-Rad, M.; Gholami, M.; Abdollahi, M. Molecular mechanisms involved in lead induced disruption of hepatic and pancreatic glucose metabolism. Environ. Toxicol. Pharmacol. 2015, 39, 16–26. [Google Scholar] [CrossRef] [PubMed]
- Tyrrell, J.B.; Hafida, S.; Stemmer, P.; Adhami, A.; Leff, T. Lead (Pb) exposure promotes diabetes in obese rodents. J. Trace Elem. Med. Biol. 2017, 39, 221–226. [Google Scholar] [CrossRef] [PubMed]
- Lanphear, B.P.; Hornung, R.; Ho, M.; Howard, C.R.; Eberly, S.; Knauf, K.; Eberle, S. Environmental lead exposure during early childhood. J. Pediatr. 2002, 140, 40–47. [Google Scholar] [CrossRef] [PubMed]
- Wadhwa, P.D.; Buss, C.; Entringer, S.; Swanson, J.M. Developmental origins of health and disease: Brief history of the approach and current focus on epigenetic mechanisms. Semin. Reprod. Med. 2009, 27, 358–368. [Google Scholar] [CrossRef] [PubMed]
- Kyle, U.G.; Pichard, C. The Dutch Famine of 1944–1945: A pathophysiological model of long-term consequences of wasting disease. Curr. Opin. Clin. Nutr. Metab. Care 2006, 9, 388–394. [Google Scholar] [CrossRef] [PubMed]
- Reynolds, R.M. Glucocorticoid excess and the developmental origins of disease: Two decades of testing the hypothesis—2012 Curt Richter Award Winner. Psychoneuroendocrinology 2013, 38, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Tolins, M.; Ruchirawat, M.; Landrigan, P. The developmental neurotoxicity of arsenic: Cognitive and behavioral consequences of early life exposure. Ann. Glob. Health 2014, 80, 303–314. [Google Scholar] [CrossRef] [PubMed]
- Hodjat, M.; Rahmani, S.; Khan, F.; Niaz, K.; Navaei-Nigjeh, M.; Mohammadi Nejad, S.; Abdollahi, M. Environmental toxicants, incidence of degenerative diseases, and therapies from the epigenetic point of view. Arch. Toxicol. 2017, 91, 2577–2597. [Google Scholar] [CrossRef] [PubMed]
- Sen, A.; Cingolani, P.; Senut, M.-C.; Land, S.; Mercado-Garcia, A.; Tellez-Rojo, M.M.; Baccarelli, A.A.; Wright, R.O.; Ruden, D.M. Lead exposure induces changes in 5-hydroxymethylcytosine clusters in CpG islands in human embryonic stem cells and umbilical cord blood. Epigenetics 2015, 10, 607–621. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sen, A.; Heredia, N.; Senut, M.-C.; Land, S.; Hollocher, K.; Lu, X.; Dereski, M.O.; Ruden, D.M. Multigenerational epigenetic inheritance in humans: DNA methylation changes associated with maternal exposure to lead can be transmitted to the grandchildren. Sci. Rep. 2015, 5, 14466. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leasure, J.L.; Giddabasappa, A.; Chaney, S.; Johnson, J.E.; Pothakos, K.; Lau, Y.S.; Fox, D.A. Low-level human equivalent gestational lead exposure produces sex-specific motor and coordination abnormalities and late-onset obesity in year-old mice. Environ. Health Perspect. 2008, 116, 355–361. [Google Scholar] [CrossRef] [PubMed]
- Faulk, C.; Barks, A.; Sánchez, B.N.; Zhang, Z.; Anderson, O.S.; Peterson, K.E.; Dolinoy, D.C. Perinatal Lead (Pb) Exposure Results in Sex-Specific Effects on Food Intake, Fat, Weight, and Insulin Response across the Murine Life-Course. PLoS ONE 2014, 9, e104273. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Faulk, C.; Barks, A.; Liu, K.; Goodrich, J.M.; Dolinoy, D.C. Early-life lead exposure results in dose- and sex-specific effects on weight and epigenetic gene regulation in weanling mice. Epigenomics 2013, 5, 487–500. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matović, V.; Buha, A.; Ðukić-Ćosić, D.; Bulat, Z. Insight into the oxidative stress induced by lead and/or cadmium in blood, liver and kidneys. Food Chem. Toxicol. 2015, 78, 130–140. [Google Scholar] [CrossRef] [PubMed]
- Fridlyand, L.; Philipson, L. Reactive species and early manifestation of insulin resistance in type 2 diabetes. Diabetes Obes. Metab. 2006, 8, 136–145. [Google Scholar] [CrossRef] [PubMed]
- Lee, D.; Lim, J.; Song, K.; Boo, Y.; Jacobs, D. Graded associations of blood lead and urinary cadmium concentrations with oxidative-stress-related markers in the U.S. population: Results from the third National Health and Nutrition Examination Survey. Environ. Health Perspect. 2006, 114, 350–354. [Google Scholar] [CrossRef] [PubMed]
- Coban, T.A.; Senturk, M.; Ciftci, M.; Kufrevioglu, O.I. Effects of some metal ions on human erythrocyte glutathione reductase: An in vitro study. Protein Pept. Lett. 2007, 14, 1027–1030. [Google Scholar] [CrossRef] [PubMed]
- Hunaiti, A.A.; Soud, M. Effect of lead concentration on the level of glutathione, glutathione S-transferase, reductase and peroxidase in human blood. Sci. Total Environ. 2000, 248, 45–50. [Google Scholar] [CrossRef]
- Bokara, K.K.; Blaylock, I.; Denise, S.B.; Bettaiya, R.; Rajanna, S.; Yallapragada, P.R. Influence of lead acetate on glutathione and its related enzymes in different regions of rat brain. J. Appl. Toxicol. 2009, 29, 452–458. [Google Scholar] [CrossRef] [PubMed]
- Knowles, S.O.; Donaldson, W.E. Dietary modification of lead toxicity: Effects on fatty acid and eicosanoid metabolism in chicks. Comp. Biochem. Physiol. C Comp. Pharmacol. Toxicol. 1990, 95, 99–104. [Google Scholar] [CrossRef]
- Lawton, L.J.; Donaldson, W.E. Lead-induced tissue fatty acid alterations and lipid peroxidation. Biol. Trace Elem. Res. 1991, 28, 83–97. [Google Scholar] [CrossRef] [PubMed]
- Ribarov, S.R.; Benov, L.C. Relationship between the hemolytic action of heavy metals and lipid peroxidation. Biochim. Biophys. Acta 1981, 640, 721–726. [Google Scholar] [CrossRef]
- Ribarov, S.R.; Benov, L.C.; Benchev, I.C. The effect of lead on hemoglobin-catalyzed lipid peroxidation. Biochim. Biophys. Acta 1981, 664, 453–459. [Google Scholar] [CrossRef]
- Ribarov, S.R.; Bochev, P.G. Lead-hemoglobin interaction as a possible source of reactive oxygen species—A chemiluminescent study. Arch. Biochem. Biophys. 1982, 213, 288–292. [Google Scholar] [CrossRef]
- Godwin, H.A. The biological chemistry of lead. Curr. Opin. Chem. Biol. 2001, 5, 223–227. [Google Scholar] [CrossRef]
- Mitchell, R.A.; Drake, J.E.; Wittlin, L.A.; Rejent, T.A. Erythrocyte porphobilinogen synthase (delta-aminolaevulinate dehydratase) activity: A reliable and quantitative indicator of lead exposure in humans. Clin. Chem. 1977, 23, 105–111. [Google Scholar] [PubMed]
- Bechara, E.J. Oxidative stress in acute intermittent porphyria and lead poisoning may be triggered by 5-aminolevulinic acid. Braz. J. Med. Biol. Res. 1996, 29, 841–851. [Google Scholar] [PubMed]
- Monteiro, H.P.; Abdalla, D.S.; Augusto, O.; Bechara, E.J. Free radical generation during delta-aminolevulinic acid autoxidation: Induction by hemoglobin and connections with porphyrinpathies. Arch. Biochem. Biophys. 1989, 271, 206–216. [Google Scholar] [CrossRef]
- Monteiro, H.P.; Abdalla, D.S.; Faljoni-Alàrio, A.; Bechara, E.J. Generation of active oxygen species during coupled autoxidation of oxyhemoglobin and delta-aminolevulinic acid. Biochim. Biophys. Acta 1986, 881, 100–106. [Google Scholar] [CrossRef]
- Ercal, N.; Gurer-Orhan, H.; Aykin-Burns, N. Toxic metals and oxidative stress part I: Mechanisms involved in metal-induced oxidative damage. Curr. Top. Med. Chem. 2001, 1, 529–539. [Google Scholar] [CrossRef] [PubMed]
- Howard, J.K. Human erythrocyte glutathione reductase and glucose 6-phosphate dehydrogenase activities in normal subjects and in persons exposed to lead. Clin. Sci. Mol. Med. 1974, 47, 515–520. [Google Scholar] [CrossRef] [PubMed]
- Othman, A.I.; El Missiry, M.A. Role of selenium against lead toxicity in male rats. J. Biochem. Mol. Toxicol. 1998, 12, 345–349. [Google Scholar] [CrossRef]
- Cheng, Y.-J.; Liu, M.-Y. Modulation of tumor necrosis factor-alpha and oxidative stress through protein kinase C and P42/44 mitogen-activated protein kinase in lead increases lipopolysaccharide-induced liver damage in rats. Shock 2005, 24, 188–193. [Google Scholar] [CrossRef] [PubMed]
- Robertson, R.P. Oxidative stress and impaired insulin secretion in type 2 diabetes. Curr. Opin. Pharmacol. 2006, 6, 615–619. [Google Scholar] [CrossRef] [PubMed]
- Evans, J.L.; Goldfine, I.D.; Maddux, B.A.; Grodsky, G.M. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 2003, 52, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Robertson, R.P.; Harmon, J.; Tran, P.O.; Tanaka, Y.; Takahashi, H. Glucose toxicity in beta-cells: Type 2 diabetes, good radicals gone bad, and the glutathione connection. Diabetes 2003, 52, 581–587. [Google Scholar] [CrossRef] [PubMed]
- Tanaka, Y.; Tran, P.O.T.; Harmon, J.; Robertson, R.P. A role for glutathione peroxidase in protecting pancreatic beta cells against oxidative stress in a model of glucose toxicity. Proc. Natl. Acad. Sci. USA 2002, 99, 12363–12368. [Google Scholar] [CrossRef] [PubMed]
- Kaneto, H.; Kajimoto, Y.; Miyagawa, J.; Matsuoka, T.; Fujitani, Y.; Umayahara, Y.; Hanafusa, T.; Matsuzawa, Y.; Yamasaki, Y.; Hori, M. Beneficial effects of antioxidants in diabetes: Possible protection of pancreatic beta-cells against glucose toxicity. Diabetes 1999, 48, 2398–2406. [Google Scholar] [CrossRef] [PubMed]
- Schanne, F.A.; Dowd, T.L.; Gupta, R.K.; Rosen, J.F. Lead increases free Ca2+ concentration in cultured osteoblastic bone cells: Simultaneous detection of intracellular free Pb2+ by 19F NMR. Proc. Natl. Acad. Sci. USA 1989, 86, 5133–5135. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Culotta, V.C.; Klee, C.B. Superoxide dismutase protects calcineurin from inactivation. Nature 1996, 383, 434–437. [Google Scholar] [CrossRef] [PubMed]
- Soleimanpour, S.A.; Crutchlow, M.F.; Ferrari, A.M.; Raum, J.C.; Groff, D.N.; Rankin, M.M.; Liu, C.; De León, D.D.; Naji, A.; Kushner, J.A.; et al. Calcineurin signaling regulates human islet beta-cell survival. J. Biol. Chem. 2010, 285, 40050–40059. [Google Scholar] [CrossRef] [PubMed]
- Kern, M.; Audesirk, G. Stimulatory and inhibitory effects of inorganic lead on calcineurin. Toxicology 2000, 150, 171–178. [Google Scholar] [CrossRef]
- Habermann, E.; Crowell, K.; Janicki, P. Lead and other metals can substitute for Ca2+ in calmodulin. Arch. Toxicol. 1983, 54, 61–70. [Google Scholar] [CrossRef] [PubMed]
- Richardt, G.; Federolf, G.; Habermann, E. The interaction of aluminum and other metal ions with calcium-calmodulin-dependent phosphodiesterase. Arch. Toxicol. 1985, 57, 257–259. [Google Scholar] [CrossRef] [PubMed]
- Richardt, G.; Federolf, G.; Habermann, E. Affinity of heavy metal ions to intracellular Ca2+-binding proteins. Biochem. Pharmacol. 1986, 35, 1331–1335. [Google Scholar] [CrossRef]
- Goering, P.L. Lead-protein interactions as a basis for lead toxicity. Neurotoxicology 1993, 14, 45–60. [Google Scholar] [PubMed]
- Denny, J.B. Molecular mechanisms, biological actions, and neuropharmacology of the growth-associated protein GAP-43. Curr. Neuropharmacol. 2006, 4, 293–304. [Google Scholar] [CrossRef] [PubMed]
- Dent, E.W.; Meiri, K.F. Distribution of phosphorylated GAP-43 (neuromodulin) in growth cones directly reflects growth cone behavior. J. Neurobiol. 1998, 35, 287–299. [Google Scholar] [CrossRef] [Green Version]
- Di Luca, M.; Pastorino, L.; Raverdino, V.; De Graan, P.N.; Caputi, A.; Gispen, W.H.; Cattabeni, F. Determination of the endogenous phosphorylation state of B-50/GAP-43 and neurogranin in different brain regions by electrospray mass spectrometry. FEBS Lett. 1996, 389, 309–313. [Google Scholar] [CrossRef] [Green Version]
- Gerendasy, D. Homeostatic tuning of Ca2+ signal transduction by members of the calpacitin protein family. J. Neurosci. Res. 1999, 58, 107–119. [Google Scholar] [CrossRef]
- Kubota, Y.; Putkey, J.A.; Shouval, H.Z.; Waxham, M.N. IQ-motif proteins influence intracellular free Ca2+ in hippocampal neurons through their interactions with calmodulin. J. Neurophysiol. 2008, 99, 264–276. [Google Scholar] [CrossRef] [PubMed]
- Kubota, Y.; Putkey, J.A.; Waxham, M.N. Neurogranin controls the spatiotemporal pattern of postsynaptic Ca2+/CaM signaling. Biophys. J. 2007, 93, 3848–3859. [Google Scholar] [CrossRef] [PubMed]
- Bayés, A.; Grant, S.G.N. Neuroproteomics: Understanding the molecular organization and complexity of the brain. Nat. Rev. Neurosci. 2009, 10, 635–646. [Google Scholar] [CrossRef] [PubMed]
- Long, G.J.; Rosen, J.F.; Schanne, F.A. Lead activation of protein kinase C from rat brain. Determination of free calcium, lead, and zinc by 19F NMR. J. Biol. Chem. 1994, 269, 834–837. [Google Scholar] [PubMed]
- Tomsig, J.L.; Suszkiw, J.B. Multisite interactions between Pb2+ and protein kinase C and its role in norepinephrine release from bovine adrenal chromaffin cells. J. Neurochem. 1995, 64, 2667–2673. [Google Scholar] [CrossRef] [PubMed]
- Markovac, J.; Goldstein, G.W. Picomolar concentrations of lead stimulate brain protein kinase C. Nature 1988, 334, 71–73. [Google Scholar] [CrossRef] [PubMed]
- Markovac, J.; Goldstein, G.W. Lead activates protein kinase C in immature rat brain microvessels. Toxicol. Appl. Pharmacol. 1988, 96, 14–23. [Google Scholar] [CrossRef]
- Tessitore, L.; Perletti, G.P.; Sesca, E.; Pani, P.; Dianzani, M.U.; Piccinini, F. Protein kinase C isozyme pattern in liver hyperplasia. Biochem. Biophys. Res. Commun. 1994, 205, 208–214. [Google Scholar] [CrossRef] [PubMed]
- Kim, K.; Annadata, M.; Goldstein, G.W.; Bressler, J.P. Induction of c-fos mRNA by lead in PC 12 cells. Int. J. Dev. Neurosci. 1997, 15, 175–182. [Google Scholar] [CrossRef]
- Matthies, H.J.; Palfrey, H.C.; Hirning, L.D.; Miller, R.J. Down regulation of protein kinase C in neuronal cells: Effects on neurotransmitter release. J. Neurosci. 1987, 7, 1198–1206. [Google Scholar] [CrossRef] [PubMed]
- Nihei, M.K.; McGlothan, J.L.; Toscano, C.D.; Guilarte, T.R. Low level Pb (2+) exposure affects hippocampal protein kinase C gamma gene and protein expression in rats. Neurosci. Lett. 2001, 298, 212–216. [Google Scholar] [CrossRef]
- Panda, S.; Antoch, M.; Miller, B.; Su, A.; Schook, A.; Straume, M.; Schultz, P.; Kay, S.; Takahashi, J.; Hogenesch, J. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 2002, 109, 307–320. [Google Scholar] [CrossRef]
- Oishi, K.; Atsumi, G.; Sugiyama, S.; Kodomari, I.; Kasamatsu, M.; Machida, K.; Ishida, N. Disrupted fat absorption attenuates obesity induced by a high-fat diet in clock mutant mice. FEBS Lett. 2006, 580, 127–130. [Google Scholar] [CrossRef] [PubMed]
- Rudic, R.; McNamara, P.; Curtis, A.; Boston, R.; Panda, S.; Hogenesch, J.; Fitzgerald, G. BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS. Biol. 2004, 2, e377. [Google Scholar] [CrossRef] [PubMed]
- Turek, F.W.; Joshu, C.; Kohsaka, A.; Lin, E.; Ivanova, G.; McDearmon, E.; Laposky, A.; Losee-Olson, S.; Easton, A.; Jensen, D.R.; et al. Obesity and metabolic syndrome in circadian clock mutant mice. Science 2005, 308, 1043–1045. [Google Scholar] [CrossRef] [PubMed]
- Yin, L. The Orphan Nuclear Receptor Rev-erb Recruits the N-CoR/Histone Deacetylase 3 Corepressor to Regulate the Circadian Bmal1 Gene. Mol. Endocrinol. 2005, 19, 1452–1459. [Google Scholar] [CrossRef] [PubMed]
- Raghuram, S.; Stayrook, K.; Huang, P.; Rogers, P.; Nosie, A.; McClure, D.; Burris, L.; Khorasanizadeh, S.; Burris, T.; Rastinejad, F. Identification of heme as the ligand for the orphan nuclear receptors REV-ERBalpha and REV-ERBbeta. Nat. Struct. Mol. Biol. 2007, 14, 1207–1213. [Google Scholar] [CrossRef] [PubMed]
- Yin, L.; Wu, N.; Curtin, J.C.; Qatanani, M.; Szwergold, N.R.; Reid, R.A.; Waitt, G.M.; Parks, D.J.; Pearce, K.H.; Wisely, G.B.; et al. Rev-erbalpha, a heme sensor that coordinates metabolic and circadian pathways. Science 2007, 318, 1786–1789. [Google Scholar] [CrossRef] [PubMed]
- Wu, N.; Yin, L.; Hanniman, E.A.; Joshi, S.; Lazar, M.A. Negative feedback maintenance of heme homeostasis by its receptor, Rev-erbalpha. Genes Dev. 2009, 23, 2201–2209. [Google Scholar] [CrossRef] [PubMed]
- Burke, L.; Downes, M.; Laudet, V.; Muscat, G. Identification and characterization of a novel corepressor interaction region in RVR and Rev-erbA alpha. Mol. Endocrinol. 1998, 12, 248–262. [Google Scholar] [PubMed]
- Santos, J.; Fontanellas, A.; Moran, M.; Enriquez de Salamanca, R. Nonsynergic effect of ethanol and lead on heme metabolism in rats. Ecotoxicol. Environ. Saf. 1999, 43, 98–102. [Google Scholar] [CrossRef] [PubMed]
- Kang, H.G.; Jeong, S.H.; Cho, M.R.; Cho, J.H.; Bischoff, K. Time-dependent changes in lead and delta-aminolevulinic acid after subchronic lead exposure in rats. Hum. Exp. Toxicol. 2009, 28, 647–654. [Google Scholar] [CrossRef] [PubMed]
- Grandjean, P. Even low-dose lead exposure is hazardous. Lancet 2010, 376, 855–856. [Google Scholar] [CrossRef]
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Leff, T.; Stemmer, P.; Tyrrell, J.; Jog, R. Diabetes and Exposure to Environmental Lead (Pb). Toxics 2018, 6, 54. https://doi.org/10.3390/toxics6030054
Leff T, Stemmer P, Tyrrell J, Jog R. Diabetes and Exposure to Environmental Lead (Pb). Toxics. 2018; 6(3):54. https://doi.org/10.3390/toxics6030054
Chicago/Turabian StyleLeff, Todd, Paul Stemmer, Jannifer Tyrrell, and Ruta Jog. 2018. "Diabetes and Exposure to Environmental Lead (Pb)" Toxics 6, no. 3: 54. https://doi.org/10.3390/toxics6030054
APA StyleLeff, T., Stemmer, P., Tyrrell, J., & Jog, R. (2018). Diabetes and Exposure to Environmental Lead (Pb). Toxics, 6(3), 54. https://doi.org/10.3390/toxics6030054