Perinatal Exposure to a High-Fat Diet Is Associated with Reduced Hepatic Sympathetic Innervation in One-Year Old Male Japanese Macaques

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Grant, Wilmon F ^a,b   Nicol, Lindsey E ^a,b   Thorn, Stephanie R ^d   Grove, Kevin L ^c   Friedman, Jacob E ^d   Marks, Daniel L ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d Children's Hospital Colorado   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN; NEUROPEPTIDE Y;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARBOHYDRATE ANALYSIS; CHROMATIN STRUCTURE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; FEMALE; FETUS; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; LIPID DIET; LIVER STRUCTURE; MACACA; MALE; NEUROANATOMY; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRENATAL EXPOSURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SYMPATHETIC INNERVATION; SYMPATHETIC NERVE; UPREGULATION;

ANIMALS; APOPTOSIS; CYTOKINES; DIET, HIGH-FAT; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOSE TRANSPORTER TYPE 2; GLYCOGEN; HEPATITIS; INFLAMMATION MEDIATORS; LIVER; MACACA; MALE; MATERNAL-FETAL EXCHANGE; NEUROPEPTIDE Y; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RECEPTORS, NEUROPEPTIDE Y; RECEPTORS, NICOTINIC; SYMPATHETIC FIBERS, POSTGANGLIONIC; SYMPATHETIC NERVOUS SYSTEM; TYROSINE 3-MONOOXYGENASE;

ANIMALIA; MACACA; PRIMATES;

EID: 84868159715     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048119     Document Type: Article

References (52)

1. Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, et al. (1991) Fetal and infant growth and impaired glucose tolerance at age 64. Bmj 303: 1019-1022.
2. Barker DJ, Osmond C, Law CM, (1989) The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J Epidemiol Community Health 43: 237-240.
3. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME, (1989) Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. Bmj 298: 564-567.
4. Dabelea D, Hanson RL, Lindsay RS, Pettitt DJ, Imperatore G, et al. (2000) Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes 49: 2208-2211.
5. Freinkel N, (1980) Banting Lecture 1980. Of pregnancy and progeny. Diabetes 29: 1023-1035.
6. Mokdad AH, Serdula MK, Dietz WH, Bowman BA, Marks JS, et al. (1999) The spread of the obesity epidemic in the United States, 1991-1998. Jama 282: 1519-1522.
7. Ogden CL, Flegal KM, Carroll MD, Johnson CL, (2002) Prevalence and trends in overweight among US children and adolescents, 1999-2000. Jama 288: 1728-1732.
8. Di Cianni G, Miccoli R, Volpe L, Lencioni C, Ghio A, et al. (2005) Maternal triglyceride levels and newborn weight in pregnant women with normal glucose tolerance. Diabet Med 22: 21-25.
9. Frias AE, Morgan TK, Evans AE, Rasanen J, Oh KY, et al. (2011) Maternal high-fat diet disturbs uteroplacental hemodynamics and increases the frequency of stillbirth in a nonhuman primate model of excess nutrition. Endocrinology 152: 2456-2464.
10. Aagaard-Tillery KM, Grove K, Bishop J, Ke X, Fu Q, et al. (2008) Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 41: 91-102.
11. Grant WF, Gillingham MB, Batra AK, Fewkes NM, Comstock SM, et al. (2011) Maternal High Fat Diet is Associated With Decreased Plasma n-3 Fatty Acids and Fetal Hepatic Apoptosis in Nonhuman Primates. PLoS One 6(2): e17261.
12. McCurdy CE, Bishop JM, Williams SM, Grayson BE, Smith SM, et al. (2009) Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. The Journal of Clinical Investigation 119: 323-335.
13. Suter M, Bocock P, Showalter L, Hu M, Shope C, et al. (2011) Epigenomics: maternal high-fat diet exposure in utero disrupts peripheral circadian gene expression in nonhuman primates. Faseb J.
14. Grayson BE, Allen SE, Billes SK, Williams SM, Smith MS, et al. (2006) Prenatal development of hypothalamic neuropeptide systems in the nonhuman primate. Neuroscience 143: 975-986.
15. Sullivan EL, Grayson B, Takahashi D, Robertson N, Maier A, et al. (2010) Chronic consumption of a high-fat diet during pregnancy causes perturbations in the serotonergic system and increased anxiety-like behavior in nonhuman primate offspring. J Neurosci 30: 3826-3830.
16. Shimazu T, (1962) The effect of electric stimulation of hypothalamus on rabbit liver tryptophan pyrrolase. Biochim Biophys Acta 65: 373-375.
17. Shimazu T, (1967) Glycogen synthetase activity in liver: regulation by the autonomic nerves. Science 156: 1256-1257.
18. Shimazu T, Fukuda A, (1965) Increased activities of glycogenolytic enzymes in liver after splanchnic-nerve stimulation. Science 150: 1607-1608.
19. Shimazu T, Fukuda A, Ban T, (1966) Reciprocal influences of the ventromedial and lateral hypothalamic nuclei on blood glucose level and liver glycogen content. Nature 210: 1178-1179.
20. Yi CX, Serlie MJ, Ackermans MT, Foppen E, Buijs RM, et al. (2009) A major role for perifornical orexin neurons in the control of glucose metabolism in rats. Diabetes 58: 1998-2005.
21. van den Hoek AM, van Heijningen C, Schroder-van der Elst JP, Ouwens DM, Havekes LM, et al. (2008) Intracerebroventricular administration of neuropeptide Y induces hepatic insulin resistance via sympathetic innervation. Diabetes 57: 2304-2310.
22. La Fleur SE, Kalsbeek A, Wortel J, Buijs RM, (1999) A suprachiasmatic nucleus generated rhythm in basal glucose concentrations. J Neuroendocrinol 11: 643-652.
23. Yi CX, la Fleur SE, Fliers E, Kalsbeek A, (2010) The role of the autonomic nervous liver innervation in the control of energy metabolism. Biochim Biophys Acta 1802: 416-431.
24. Forssmann WG, Ito S, (1977) Hepatocyte innervation in primates. J Cell Biol 74: 299-313.
25. Nobin A, Baumgarten HG, Falck B, Ingemansson S, Moghimzadeh E, et al. (1978) Organization of the sympathetic innervation in liver tissue from monkey and man. Cell Tissue Res 195: 371-380.
26. Glavas MM, Grayson BE, Allen SE, Copp DR, Smith MS, et al. (2008) Characterization of brainstem peptide YY (PYY) neurons. J Comp Neurol 506: 194-210.
27. Sanchez-Gonzalez MA, Garcia-Cabezas MA, Rico B, Cavada C, (2005) The primate thalamus is a key target for brain dopamine. J Neurosci 25: 6076-6083.
28. Burcelin R, Dolci W, Thorens B, (2000) Glucose sensing by the hepatoportal sensor is GLUT2-dependent: in vivo analysis in GLUT2-null mice. Diabetes 49: 1643-1648.
29. Burt AD, Tiniakos D, MacSween RN, Griffiths MR, Wisse E, et al. (1989) Localization of adrenergic and neuropeptide tyrosine-containing nerves in the mammalian liver. Hepatology 9: 839-845.
30. Goehler LE, Sternini C, (1991) Neuropeptide Y immunoreactivity in the mammalian liver: pattern of innervation and coexistence with tyrosine hydroxylase immunoreactivity. Cell Tissue Res 265: 287-295.
31. Barzilaym JI, Freedland ES, (2003) Inflammation and its relationship to insulin resistance, type 2 diabetes mellitus, and endothelial dysfunction. Metab Syndr Relat Disord 1: 55-67.
32. Berg AH, Scherer PE, (2005) Adipose tissue, inflammation, and cardiovascular disease. Circ Res 96: 939-949.
33. Hotamisligil GS, (2006) Inflammation and metabolic disorders. Nature 444: 860-867.
34. Cai D, Yuan M, Frantz DF, Melendez PA, Hansen L, et al. (2005) Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat Med 11: 183-190.
35. Patel DN, King CA, Bailey SR, Holt JW, Venkatachalam K, et al. (2007) Interleukin-17 stimulates C-reactive protein expression in hepatocytes and smooth muscle cells via p38 MAPK and ERK1/2-dependent NF-kappaB and C/EBPbeta activation. J Biol Chem 282: 27229-27238.
36. Browning JL, Ngam-ek A, Lawton P, DeMarinis J, Tizard R, et al. (1993) Lymphotoxin beta, a novel member of the TNF family that forms a heteromeric complex with lymphotoxin on the cell surface. Cell 72: 847-856.
37. Granger GA, Williams TW, (1968) Lymphocyte cytotoxicity in vitro: activation and release of a cytotoxic factor. Nature 218: 1253-1254.
38. Granger SW, Ware CF (2003) Lymphotoxins. In: Thomson AW, Lotze, M.T., editor. The Cytokine Handbook. 4th ed. London: Elsevier Science Ltd. 825-835.
39. Yoshikawa H, Kurokawa M, Ozaki N, Nara K, Atou K, et al. (2006) Nicotine inhibits the production of proinflammatory mediators in human monocytes by suppression of I-kappaB phosphorylation and nuclear factor-kappaB transcriptional activity through nicotinic acetylcholine receptor alpha7. Clin Exp Immunol 146: 116-123.
40. de Jonge WJ, van der Zanden EP, The FO, Bijlsma MF, van Westerloo DJ, et al. (2005) Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway. Nat Immunol 6: 844-851.
41. Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, et al. (2000) Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405: 458-462.
42. Poynard T, Mathurin P, Lai CL, Guyader D, Poupon R, et al. (2003) A comparison of fibrosis progression in chronic liver diseases. J Hepatol 38: 257-265.
43. Harada H, Pavlick KP, Hines IN, Hoffman JM, Bharwani S, et al. (2001) Selected contribution: Effects of gender on reduced-size liver ischemia and reperfusion injury. J Appl Physiol 91: 2816-2822.
44. Bertola A, Bonnafous S, Anty R, Patouraux S, Saint-Paul MC, et al. (2010) Hepatic expression patterns of inflammatory and immune response genes associated with obesity and NASH in morbidly obese patients. PLoS One 5: e13577.
45. Francavilla A, Eagon PK, DiLeo A, Polimeno L, Panella C, et al. (1986) Sex hormone-related functions in regenerating male rat liver. Gastroenterology 91: 1263-1270.
46. Tiniakos DG, Mathew J, Kittas C, Burt AD, (2008) Ontogeny of human intrahepatic innervation. Virchows Arch 452: 435-442.
47. Tiniakos DG (1996) Development of intrahepatic nerves in human liver. In: Shimazu T, editor. Liver innervation and the control of hepatic function. London: John Libbey & Company Ltd. 23-29.
48. Delalande JM, Milla PJ, Burns AJ, (2004) Hepatic nervous system development. Anat Rec A Discov Mol Cell Evol Biol 280: 848-853.
49. Ding WG, Kitasato H, Kimura H, (1997) Development of neuropeptide Y innervation in the liver. Microsc Res Tech 39: 365-371.
50. Feher E, Fodor M, Gorcs T, Feher J, Vallent K, (1991) Immunohistochemical distribution of neuropeptide Y and catecholamine-synthesizing enzymes in nerve fibers of the human liver. Digestion 50: 194-201.
51. Grayson BE, Levasseur PR, Williams SM, Smith MS, Marks DL, et al. (2010) Changes in melanocortin expression and inflammatory pathways in fetal offspring of nonhuman primates fed a high-fat diet. Endocrinology 151: 1622-1632.
52. Fan L, Lindsley SR, Comstock SM, Takahashi DL, Evans AE, et al. (2012) Maternal high-fat diet impacts endothelial function in nonhuman primate offspring. Int J Obes (Lond): 1-9.