DOI QR코드

DOI QR Code

Effects of maternal cigarette smoke exposure on the progression of nonalcoholic steatohepatitis in offspring mice

  • Daram, Yang (Biosafety Research Institute and Laboratory of Veterinary Pathology, College of Veterinary Medicine, Jeonbuk National University) ;
  • Jong Won, Kim (Biosafety Research Institute and Laboratory of Veterinary Pathology, College of Veterinary Medicine, Jeonbuk National University) ;
  • Hyuneui, Jeong (Biosafety Research Institute and Laboratory of Veterinary Pathology, College of Veterinary Medicine, Jeonbuk National University) ;
  • Min Seok, Kim (Inhalation Toxicology Center, Jeonbuk Department of Inhalation Research, Korea Institute of Toxicology) ;
  • Chae Woong, Lim (Biosafety Research Institute and Laboratory of Veterinary Pathology, College of Veterinary Medicine, Jeonbuk National University) ;
  • Kyuhong, Lee (Inhalation Toxicology Center, Jeonbuk Department of Inhalation Research, Korea Institute of Toxicology) ;
  • Bumseok, Kim (Biosafety Research Institute and Laboratory of Veterinary Pathology, College of Veterinary Medicine, Jeonbuk National University)
  • 투고 : 2022.05.30
  • 심사 : 2022.08.22
  • 발행 : 2023.01.15

초록

Cigarette smoke (CS) is a dominant carcinogenic agent in a variety of human cancers. CS exposure during pregnancy can adversely affect the fetus. Non-alcoholic fatty liver disease (NAFLD) is considered as a hepatic manifestation of a metabolic disorder, and ranges from simple steatosis to cirrhosis leading to hepatocellular carcinoma. Non-alcoholic steatohepatitis (NASH) is a more severe phase of NAFLD. Recently, there is increasing apprehension about the CS-related chronic liver diseases. Therefore, we examined whether maternal CS exposure could affect the pathogenesis of NASH in offspring. Mainstream CS (MSCS) was exposed to pregnant C57BL/6 mice via nose-only inhalation for 2 h/day, 5 days/week for 2 weeks from day 6 to 17 of gestation at 0, 300, or 600 ㎍/L. Three-week-old male offspring mice were fed methionine and choline-supplemented (MCS) diet or methionine and choline-deficient including high-fat (MCDHF) diet for 6 weeks to induce NASH. Maternal MSCS exposure increased the severity of NASH by increasing serum alanine aminotransferase (ALT) and aspartate aminotransferase (AST) levels, hepatic total cholesterol (TC) and triglyceride (TG) levels, pro-inflammation, fibrosis, and steatosis in offspring mice. Especially, maternal MSCS exposure significantly downregulated the phosphorylation of AMP-activated protein kinase (AMPK) in MCDHF diet-fed offspring mice. Subsequently, the protein levels of sterol regulatory element-binding protein (SREBP)-1c and stearoyl-CoA desaturase-1 (SCD1) were upregulated by maternal MSCS exposure. In conclusion, maternal MSCS exposure exacerbates the progression of NASH by modulating lipogenesis on offspring mice.

키워드

과제정보

This study was supported by grants (No. 21203MFDS318) from the Ministry of Food and Drug Safety, Republic of Korea and the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) (HI20C0209) (J-W.K.) funded by the Ministry of Health & Welfare, Republic of Korea.

참고문헌

  1. Anstee QM, Day CP (2013) The genetics of NAFLD. Nat Rev Gastroenterol Hepatol 10:645-655. https://doi.org/10.1038/nrgastro.2013.182
  2. Younossi ZM, Otgonsuren M, Henry L, Venkatesan C, Mishra A, Erario M, Hunt S (2015) Association of nonalcoholic fatty liver disease (NAFLD) with hepatocellular carcinoma (HCC) in the United States from 2004 to 2009. Hepatology 62:1723-1730. https://doi.org/10.1002/hep.28123
  3. Peverill W, Powell LW, Skoien R (2014) Evolving concepts in the pathogenesis of NASH: beyond steatosis and inflammation. Int J Mol Sci 15:8591-8638. https://doi.org/10.3390/ijms15058591
  4. Tilg H, Moschen AR (2010) Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 52:1836-1846. https://doi.org/10.1002/hep.24001
  5. Min HK, Kapoor A, Fuchs M, Mirshahi F, Zhou H, Maher J, Kellum J, Warnick R, Contos MJ, Sanyal AJ (2012) Increased hepatic synthesis and dysregulation of cholesterol metabolism is associated with the severity of nonalcoholic fatty liver disease. Cell metab 15:665-674. https://doi.org/10.1016/j.cmet.2012.04.004
  6. Tomita K, Teratani T, Suzuki T, Shimizu M, Sato H, Narimatsu K, Okada Y, Kurihara C, Irie R, Yokoyama H et al (2014) Free cholesterol accumulation in hepatic stellate cells: mechanism of liver fibrosis aggravation in nonalcoholic steatohepatitis in mice. Hepatology 59:154-169. https://doi.org/10.1002/hep.26604
  7. Ioannou GN (2016) The role of cholesterol in the pathogenesis of NASH. Trends Endocrinol Metab 27:84-95. https://doi.org/10.1016/j.tem.2015.11.008
  8. Sopori ML, Kozak W (1998) Immunomodulatory effects of cigarette smoke. J Neuroimmunol 83:148-156. https://doi.org/10.1016/s0165-5728(97)00231-2
  9. Saha SP, Bhalla DK, Whayne TF, Gairola CG (2007) Cigarette smoke and adverse health effects: an overview of research trends and future needs. Int J Angiol 16:77-83. https://doi.org/10.1055/s-0031-1278254
  10. Jaimes EA, Tian RX, Raij L (2007) Nicotine: the link between cigarette smoking and the progression of renal injury? Am J Physiol Heart Circ Physiol 292:H76-H82. https://doi.org/10.1152/ajpheart.00693.2006
  11. Cena H, Fonte ML, Turconi G (2011) Relationship between smoking and metabolic syndrome. Nutr Rev 69:745-753. https://doi.org/10.1111/j.1753-4887.2011.00446.x
  12. Azzalini L, Ferrer E, Ramalho LN, Moreno M, Dominguez M, Colmenero J, Peinado VI, Barbera JA, Arroyo V, Gines P et al (2010) Cigarette smoking exacerbates nonalcoholic fatty liver disease in obese rats. Hepatology 51:1567-1576. https://doi.org/10.1002/hep.23516
  13. Yuan H, Shyy JYJ, Martins-Green M (2009) Second-hand smoke stimulates lipid accumulation in the liver by modulating AMPK and SREBP-1. J Hepatol 51:535-547. https://doi.org/10.1016/j.jhep.2009.03.026
  14. Park S, Kim JW, Yun H, Choi SJ, Lee SH, Choi KC, Lim CW, Lee K, Kim B (2016) Mainstream cigarette smoke accelerates the progression of nonalcoholic steatohepatitis by modulating Kupffer cell-mediated hepatocellular apoptosis in adolescent mice. Toxicol Lett 256:53-63. https://doi.org/10.1016/j.toxlet.2016.05.012
  15. Larcombe AN, Foong RE, Berry LJ, Zosky GR, Sly PD (2011) In utero cigarette smoke exposure impairs somatic and lung growth in BALB/c mice. Eur Respir J 38:932-938. https://doi.org/10.1183/09031936.00156910
  16. Eyring KR, Pedersen BS, Yang IV, Schwartz DA (2015) In utero cigarette smoke affects allergic airway disease but does not alter the lung methylome. PLoS ONE 10:e0144087. https://doi.org/10.1371/journal.pone.0144087
  17. Grydeland TB, Dirksen A, Coxson HO, Pillai SG, Sharma S, Eide GE, Gulsvik A, Bakke PS (2009) Quantitative computed tomography: emphysema and airway wall thickness by sex, age and smoking. Eur Respir J 34:858-865. https://doi.org/10.1183/09031936.00167908
  18. Wu ZX, Hunter DD, Kish VL, Benders KM, Batchelor TP, Dey RD (2009) Prenatal and early, but not late, postnatal exposure of mice to sidestream tobacco smoke increases airway hyperresponsiveness later in life. Environ Health Perspect 117:1434-1440. https://doi.org/10.1289/ehp.0800511
  19. Chou HC, Chen CM (2014) Maternal nicotine exposure during gestation and lactation induces cardiac remodeling in rat offspring. Reprod Toxicol 50:4-10. https://doi.org/10.1016/j.reprotox.2014.09.013
  20. Xiao D, Dasgupta C, Li Y, Huang X, Zhang L (2014) Perinatal nicotine exposure increases angiotensin II receptor-mediated vascular contractility in adult offspring. PLoS ONE 9:e108161. https://doi.org/10.1371/journal.pone.0108161
  21. Wongtrakool C, Wang N, Hyde DM, Roman J, Spindel ER (2012) Prenatal nicotine exposure alters lung function and airway geometry through α7 nicotinic receptors. Am J Respir Cell Mol Biol 46:695-702. https://doi.org/10.1165/rcmb.2011-0028OC
  22. Huang LT, Chou HC, Lin CM, Yeh TF, Chen CM (2014) Maternal nicotine exposure exacerbates neonatal hyperoxia-induced lung fibrosis in rats. Neonatology 106:94-101. https://doi.org/10.1159/000362153
  23. Chan YL, Saad S, Pollock C, Oliver B, Al-Odat I, Zaky AA, Jones N, Chen H (2016) Impact of maternal cigarette smoke exposure on brain inflammation and oxidative stress in male mice offspring. Sci Rep 6:1-12. https://doi.org/10.1038/srep25881
  24. Hamdi Y, Madfai H, Belhareth R, Mokni M, Masmoudi-Kouki O, Amri M (2016) Prenatal exposure to cigarette smoke enhances oxidative stress in astrocytes of neonatal rat. Toxicol Mech Methods 26:231-237. https://doi.org/10.3109/15376516.2016.1156205
  25. Al-Odat I, Chen H, Chan YL, Amgad S, Wong MG, Gill A, Pollock C, Saad S (2014) The impact of maternal cigarette smoke exposure in a rodent model on renal development in the offspring. PLoS ONE 9:e103443. https://doi.org/10.1371/journal.pone.0103443
  26. Stangenberg S, Nguyen LT, Chen H, Al-Odat I, Killingsworth MC, Gosnell ME, Anwer AG, Goldys EM, Pollock CA, Saad S (2015) Oxidative stress, mitochondrial perturbations and fetal programming of renal disease induced by maternal smoking. Int J Biochem Cell Biol 64:81-90. https://doi.org/10.1016/j.biocel.2015.03.017
  27. Nguyen LT, Stangenberg S, Chen H, Al-Odat I, Chan YL, Gosnell ME, Anwer AG, Goldys EM, Pollock CA, Saad S (2015) L-Carnitine reverses maternal cigarette smoke exposure-induced renal oxidative stress and mitochondrial dysfunction in mouse offspring. Am J Physiol Renal Physiol 308:F689-F696. https://doi.org/10.1152/ajprenal.00417.2014
  28. Balansky R, Ganchev G, Iltcheva M, Nikolov M, Steele VE, De Flora S (2012) Differential carcinogenicity of cigarette smoke in mice exposed either transplacentally, early in life or in adulthood. Int J Cancer 130:1001-1010. https://doi.org/10.1002/ijc.26103
  29. Ng SP, Silverstone AE, Lai ZW, Zelikoff JT (2006) Effects of prenatal exposure to cigarette smoke on offspring tumor susceptibility and associated immune mechanisms. Toxicol Sci 89:135-144. https://doi.org/10.1093/toxsci/kfj006
  30. International Organization for Standardization (1999) Tobacco and Tobacco Products-Atmosphere for Conditioning and Testing. ISO 3402
  31. International Organization for Standardization (2012) Routine Analytical Cigarette-Smoking Machine-Definitions and Standard Conditions. ISO 3308
  32. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, Ferrell LD, Liu YC, Torbenson MS, Unalp-Arida A et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41:1313-1321. https://doi.org/10.1002/hep.20701
  33. Tessari P, Coracina A, Cosma A, Tiengo A (2009) Hepatic lipid metabolism and non-alcoholic fatty liver disease. Nutr Metab Cardiovasc Dis 19:291-302. https://doi.org/10.1016/j.numecd.2008.12.015
  34. Bradbury MW, Berk PD (2004) Lipid metabolism in hepatic steatosis. Clin Liver Dis 8:639-671. https://doi.org/10.1016/j.cld.2004.04.005
  35. Liu Q, Bengmark S, Qu S (2010) The role of hepatic fat accumulation in pathogenesis of non-alcoholic fatty liver disease (NAFLD). Lipids Health Dis 9:1-9. https://doi.org/10.1186/1476-511X-9-42
  36. Zhu X, Bian H, Wang L, Sun X, Xu X, Yan H, Xia M, Chang X, Lu Y, Li Y et al (2019) Berberine attenuates nonalcoholic hepatic steatosis through the AMPK-SREBP-1c-SCD1 pathway. Free Radic Biol Med 141:192-204. https://doi.org/10.1016/j.freeradbiomed.2019.06.019
  37. Dobrzyn P, Dobrzyn A, Miyazaki M, Cohen P, Asilmaz E, Hardie DG, Friedman JM, Ntambi JM (2004) Stearoyl-CoA desaturase 1 deficiency increases fatty acid oxidation by activating AMP-activated protein kinase in liver. Proc Natl Acad Sci USA 101:6409-6414. https://doi.org/10.1073/pnas.0401627101
  38. Lelliott C, Vidal-Puig AJ (2004) Lipotoxicity, an imbalance between lipogenesis de novo and fatty acid oxidation. Int J Obes Relat Metab Disord 28:S22-S28. https://doi.org/10.1038/sj.ijo.0802854
  39. Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, Pfaff DW (1998) Roles of estrogen receptor-α gene expression in reproduction-related behaviors in female mice. Endocrinology 139:5070-5081. https://doi.org/10.1210/endo.139.12.6357
  40. Wira CR, Rodriguez-Garcia M, Patel MV (2015) The role of sex hormones in immune protection of the female reproductive tract. Nat Rev Immunol 15:217-230. https://doi.org/10.1038/nri3819
  41. Whitacre CC (2001) Sex differences in autoimmune disease. Nat Immunol 2:777-780. https://doi.org/10.1038/ni0901-777
  42. Melgert BN, Postma DS, Kuipers I, Geerlings M, Luinge MA, Van Der Strate BWA, Kerstjens H, Timens W, Hylkema MN (2005) Female mice are more susceptible to the development of allergic airway inflammation than male mice. Clin Exp Allergy 35:1496-1503. https://doi.org/10.1111/j.1365-2222.2005.02362.x
  43. Hong J, Stubbins RE, Smith RR, Harvey AE, Nunez NP (2009) Differential susceptibility to obesity between male, female and ovariectomized female mice. Nutr J 8:1-5. https://doi.org/10.1186/1475-2891-8-11
  44. Zaren B, Lindmark G, Bakketeig L (2000) Maternal smoking affects fetal growth more in the male fetus. Paediatr Perinat Epidemiol 14:118-126. https://doi.org/10.1046/j.1365-3016.2000.00247.x
  45. Larsen LG, Clausen HV, Jonsson L (2002) Stereologic examination of placentas from mothers who smoke during pregnancy. Am J Obstet Gynecol 186:531-537. https://doi.org/10.1067/mob.2002.120481
  46. Weitzman M, Gortmaker S, Walker DK, Sobol A (1990) Maternal smoking and childhood asthma. Pediatrics 85:505-511. https://doi.org/10.1542/peds.85.4.505
  47. Weitzman M, Gortmaker S, Sobol A (1992) Maternal smoking and behavior problems of children. Pediatrics 90:342-349. https://doi.org/10.1542/peds.90.3.342
  48. Von Kries R, Toschke AM, Koletzko B, Slikker W Jr (2002) Maternal smoking during pregnancy and childhood obesity. Am J Epidemiol 156:954-961. https://doi.org/10.1093/aje/kwf128
  49. Novaes Soares P, Silva Tavares Rodrigues V, Cherem Peixoto T, Calvino C, Aparecida Miranda R, Pereira Lopes B, Peixoto-Silva N, Lopes Costa L, Claudio-Neto S, Christian Manhaes A et al (2018) Cigarette smoke during breastfeeding in rats changes glucocorticoid and vitamin D status in obese adult offspring. Int J Mol Sci 19:3084. https://doi.org/10.3390/ijms19103084
  50. Jaakkola JM, Rovio SP, Pahkala K, Viikari J, Ronnemaa T, Jula A, Niinikoski H, Mykkanen J, Juonala M, Hutri-Kahonen N et al (2021) Childhood exposure to parental smoking and life-course overweight and central obesity. Ann Med 53:208-216. https://doi.org/10.1080/07853890.2020.1853215
  51. Chiba M, Masironi R (1992) Toxic and trace elements in tobacco and tobacco smoke. Bull World Health Organ. 70:269. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2393306/
  52. Schick S, Glantz S (2005) Philip Morris toxicological experiments with fresh sidestream smoke: more toxic than mainstream smoke. Tob Control 14:396-404. https://doi.org/10.1136/tc.2005.011288
  53. Behera SN, Xian H, Balasubramanian R (2014) Human health risk associated with exposure to toxic elements in mainstream and sidestream cigarette smoke. Sci Total Environ 472:947-956. https://doi.org/10.1016/j.scitotenv.2013.11.063
  54. Wang Q, Liu S, Zhai A, Zhang B, Tian G (2018) AMPK-mediated regulation of lipid metabolism by phosphorylation. Biol Pharm Bull 41:985-993. https://doi.org/10.1248/bpb.b17-00724
  55. Horton JD, Goldstein JL, Brown MS (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109:1125-1131. https://doi.org/10.1172/JCI15593
  56. Seo MS, Hong SW, Yeon SH, Kim YM, Um KA, Kim JH, Kim HJ, Chang KC, Park SW (2014) Magnolia officinalis attenuates free fatty acid-induced lipogenesis via AMPK phosphorylation in hepatocytes. J Ethnopharmacol 157:140-148. https://doi.org/10.1016/j.jep.2014.09.031
  57. Kim E, Lee JH, Ntambi JM, Hyun CK (2011) Inhibition of stearoyl-CoA desaturase1 activates AMPK and exhibits beneficial lipid metabolic effects in vitro. Eur J Pharmacol 672:38-44. https://doi.org/10.1016/j.ejphar.2011.09.172
  58. Churg A, Dai J, Tai H, Xie C, Wright JL (2002) Tumor necrosis factor-α is central to acute cigarette smoke-induced inflammation and connective tissue breakdown. Am J Respir Crit Care Med 166:849-854. https://doi.org/10.1164/rccm.200202-097OC
  59. Castro P, Legora-Machado A, Cardilo-Reis L, Valenca S, Porto LC, Walker C, Zuany-Amorim C, Koatz VLG (2004) Inhibition of interleukin-1β reduces mouse lung inflammation induced by exposure to cigarette smoke. Eur J Pharmacol 498:279-286. https://doi.org/10.1016/j.ejphar.2004.07.047
  60. Goette A, Lendeckel U, Kuchenbecker A, Bukowska A, Peters B, Klein HU, Huth C, Rocken C (2007) Cigarette smoking induces atrial fibrosis in humans via nicotine. Heart 93:1056-1063. https://doi.org/10.1136/hrt.2005.087171
  61. Baumgartner KB, Samet JM, Stidley CA, Colby TV, Waldron JA (1997) Cigarette smoking: a risk factor for idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 155:242-248. https://doi.org/10.1164/ajrccm.155.1.9001319