Homozygous MTTP and APOB mutations may lead to hepatic steatosis and fibrosis despite metabolic differences in congenital hypocholesterolemia

Journal of Hepatology

Volumn 61, Issue 4, 2014, Pages 891-902

  Di Filippo, Mathilde ^a,b   Moulin, Philippe ^a,b   Roy, Pascal ^a,c   Samson Bouma, Marie Elisabeth ^d   Collardeau Frachon, Sophie ^a   Chebel Dumont, Sabrina ^a   Peretti, Noël ^a   Dumortier, Jérôme ^e   Zoulim, Fabien ^f   Fontanges, Thierry ^g   Parini, Rossella ^h   Rigoldi, Miriam ^h   Furlan, Francesca ^h   Mancini, Grazia ⁱ   Bonnefont Rousselot, Dominique ^j,k,l   Bruckert, Eric ^l   Schmitz, Jacques ^m   Scoazec, Jean Yves ^e   Charrière, Sybil ^a,b   Villar Fimbel, Sylvie ^a   Gottrand, Frederic ⁿ   Dubern, Béatrice ^o,p   Doummar, Diane ^o   Joly, Francesca ^q   Liard Meillon, Marie Elisabeth ^r   Lachaux, Alain ^a,c   Sassolas, Agnès ^a,b   more..

^a HOSPICES CIVILS DE LYON   (France)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITÉ LYON 1   (France)

^d INSERM   (France)

^e EDOUARD HERRIOT HOSPITAL   (France)

^f CROIX ROUSSE HOSPITAL   (France)

^g Centre Hospitalier Pierre Oudot   (France)

^h SAN GERARDO HOSPITAL   (Italy)

ⁱ ERASMUS MEDICAL CENTER   (Netherlands)

^j FACULTÉ DES SCIENCES PHARMACEUTIQUES ET BIOLOGIQUES   (France)

^k SORBONNE UNIVERSITÉ   (France)

^l PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^m HÔPITAL NECKER ENFANTS MALADES   (France)

ⁿ LILLE UNIVERSITY HOSPITAL   (France)

^o ARMAND TROUSSEAU HOSPITAL   (France)

^p CENTRE DE RECHERCHE DES CORDELIERS   (France)

^q BEAUJON HOSPITAL   (France)

^r Anatomie et Cytologie Pathologiques   (France)

more..

Author keywords

Abetalipoproteinemia; APOB; Homozygous or compound heterozygous familial hypobetalipoproteinemia; Hypocholesterolemia; Insulin resistance; Liver fibrosis; Liver steatosis; MTTP; NASH; Obesity

Indexed keywords

HIGH DENSITY LIPOPROTEIN CHOLESTEROL; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; TRIACYLGLYCEROL; APOB PROTEIN, HUMAN; APOLIPOPROTEIN B100; CARRIER PROTEIN;

ABETALIPOPROTEINEMIA; ADOLESCENT; ADULT; AGE; APOLIPOPROTEIN B GENE; ARTICLE; CHILD; CLINICAL ARTICLE; CLINICAL FEATURE; COMORBIDITY; CONTROLLED STUDY; DIARRHEA; EYE DISEASE; FAMILIAL HYPOBETALIPOPROTEINEMIA; FATTY LIVER; FEMALE; GENE; GENE MUTATION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; HYPOCHOLESTEROLEMIA; INFANT; LEAN BODY WEIGHT; LIVER FIBROSIS; MALE; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN LARGE SUBUNIT GENE; NEUROLOGIC DISEASE; OBESITY; PHENOTYPE; PREVALENCE; PRIORITY JOURNAL; TRIACYLGLYCEROL BLOOD LEVEL; BLOOD; COHORT ANALYSIS; FRANCE; GENETICS; HYPOBETALIPOPROTEINEMIAS; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; METABOLISM; NON-ALCOHOLIC FATTY LIVER DISEASE;

ABETALIPOPROTEINEMIA; ADOLESCENT; ADULT; APOLIPOPROTEIN B-100; CARRIER PROTEINS; CHOLESTEROL, HDL; COHORT STUDIES; COMORBIDITY; FEMALE; FRANCE; HUMANS; HYPOBETALIPOPROTEINEMIAS; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; MALE; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; PREVALENCE; TRIGLYCERIDES;

EID: 84926410232     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2014.05.023     Document Type: Article

References (111)

1. Gutierrez-Cirlos C, Ordonez-Sanchez ML, Tusie-Luna MT, Patterson BW, Schonfeld G, Aguilar-Salinas CA. Familial hypobetalipoproteinemia in a hospital survey: genetics, metabolism and non-alcoholic fatty liver disease. Ann Hepatol 2011; 10: 155-164.
2. Whitfield AJ, Barrett PH, van Bockxmeer FM, Burnett JR. Lipid disorders and mutations in the APOB gene. Clin Chem 2004; 50: 1725-1732.
3. Hooper AJ, van Bockxmeer FM, Burnett JR. Monogenic hypocholesterolaemic lipid disorders and apolipoprotein B metabolism. Crit Rev Clin Lab Sci 2005; 42: 515-545.
4. Tarugi P, Averna M. Hypobetalipoproteinemia: genetics, biochemistry, and clinical spectrum. Adv Clin Chem 2011; 54: 81-107.
5. Schonfeld G, Patterson BW, Yablonskiy DA, Tanoli TS, Averna M, Elias N, et al. Fatty liver in familial hypobetalipoproteinemia: triglyceride assembly into VLDL particles is affected by the extent of hepatic steatosis. J Lipid Res 2003; 44: 470-478.
6. Tanoli T, Yue P, Yablonskiy D, Schonfeld G. Fatty liver in familial hypobetalipoproteinemia: roles of the APOB defects, intra-abdominal adipose tissue, and insulin sensitivity. J Lipid Res 2004; 45: 941-947.
7. Sankatsing RR, Fouchier SW, de Haan S, Hutten BA, de Groot E, Kastelein JJ, et al. Hepatic and cardiovascular consequences of familial hypobetalipoproteinemia. Arterioscler Thromb Vasc Biol 2005; 25: 1979-1984.
8. Lonardo A, Lombardini S, Scaglioni F, Carulli L, Ricchi M, Ganazzi D, et al. Hepatic steatosis and insulin resistance: does etiology make a difference? J Hepatol 2006; 44: 190-196.
9. Schonfeld G, Yue P, Lin X, Chen Z. Fatty liver and insulin resistance: not always linked. Trans Am Clin Climatol Assoc 2008; 119: 217-223.
10. Ballestri S, Lonardo A, Losi L, Pellegrini E, Bertolotti M, Loria P. Do diabetes and obesity promote hepatic fibrosis in familial heterozygous hypobetalipoproteinemia? Intern Emerg Med 2009; 4: 71-73.
11. Amaro A, Fabbrini E, Kars M, Yue P, Schechtman K, Schonfeld G, et al. Dissociation between intrahepatic triglyceride content and insulin resis- tance in familial hypobetalipoproteinemia. Gastroenterology 2010; 139: 149-153.
12. Della Corte C, Fintini D, Giordano U, Cappa M, Brufani C, Majo F, et al. Fatty liver and insulin resistance in children with hypobetalipoproteinemia: the importance of aetiology. Clin Endocrinol (Oxf) 2013; 79: 49-54.
13. Visser ME, Lammers NM, Nederveen AJ, van der Graaf M, Heerschap A, Ackermans MT, et al. Hepatic steatosis does not cause insulin resistance in people with familial hypobetalipoproteinaemia. Diabetologia 2011; 54: 2113-2121.
14. Visser ME, Wagener G, Baker BF, Geary RS, Donovan JM, Beuers UH, et al. Mipomersen, an apolipoprotein B synthesis inhibitor, lowers low-density lipoprotein cholesterol in high-risk statin-intolerant patients: a randomized, double-blind, placebo-controlled trial. Eur Heart J 2012; 33: 1142-1149.
15. Sacks FM, Stanesa M, Hegele RA. Severe hypertriglyceridemia with pancreatitis: thirteen years' treatment with lomitapide. JAMA Intern Med 2014; 174: 443-447.
16. Visser ME, Akdim F, Tribble DL, Nederveen AJ, Kwoh TJ, Kastelein JJ, et al. Effect of apolipoprotein-B synthesis inhibition on liver triglyceride content in patients with familial hypercholesterolemia. J Lipid Res 2010; 51: 1057-1062.
17. Stein EA, Dufour R, Gagne C, Gaudet D, East C, Donovan JM, et al. Apolipoprotein B synthesis inhibition with mipomersen in heterozygous familial hypercholesterolemia: results of a randomized, double-blind, placebo-controlled trial to assess efficacy and safety as add-on therapy in patients with coronary artery disease. Circulation 2012; 126: 2283-2292.
18. Wetterau JR, Aggerbeck LP, Bouma ME, Eisenberg C, Munck A, Hermier M, et al. Absence of microsomal triglyceride transfer protein in individuals with abetalipoproteinemia. Science 1992; 258: 999-1001.
19. Rehberg EF, Samson-Bouma ME, Kienzle B, Blinderman L, Jamil H, Wetterau JR, et al. A novel abetalipoproteinemia genotype. Identification of a missense mutation in the 97-kDa subunit of the microsomal triglyceride transfer protein that prevents complex formation with protein disulfide isomerase. J Biol Chem 1996; 271: 29945-29952.
20. Chardon L, Sassolas A, Dingeon B, Michel-Calemard L, Bovier-Lapierre M, Moulin P, et al. Identification of two novel mutations and long-term followup in abetalipoproteinemia: a report of four cases. Eur J Pediatr 2009; 168: 983-989.
21. Di Filippo M, Crehalet H, Samson-Bouma ME, Bonnet V, Aggerbeck LP, Rabes JP, et al. Molecular and functional analysis of two new MTTP gene mutations in an atypical case of abetalipoproteinemia. J Lipid Res 2012; 53: 548-555.
22. Charcosset M, Sassolas A, Peretti N, Roy CC, Deslandres C, Sinnett D, et al. Anderson or chylomicron retention disease: molecular impact of five mutations in the SAR1B gene on the structure and the functionality of Sar1b protein. Mol Genet Metab 2008; 93: 74-84.
23. Kane JP, Hardman DA, Paulus HE. Heterogeneity of apolipoprotein B: isolation of a new species from human chylomicrons. Proc Natl Acad Sci U S A 1980; 77: 2465-2469.
24. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28: 412-419.
25. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005; 41: 1313-1321.
26. Illingworth DR, Connor WE, Lin DS, Diliberti J. Lipid metabolism in abetalipoproteinemia: a study of cholesterol absorption and sterol balance in two patients. Gastroenterology 1980; 78: 68-75.
27. Sharp D, Blinderman L, Combs KA, Kienzle B, Ricci B, Wager-Smith K, et al. Cloning and gene defects in microsomal triglyceride transfer protein associated with abetalipoproteinaemia. Nature 1993; 365: 65-69.
28. Shoulders CC, Brett DJ, Bayliss JD, Narcisi TM, Jarmuz A, Grantham TT, et al. Abetalipoproteinemia is caused by defects of the gene encoding the 97 kDa subunit of a microsomal triglyceride transfer protein. Hum Mol Genet 1993; 2: 2109-2116.
29. Narcisi TM, Shoulders CC, Chester SA, Read J, Brett DJ, Harrison GB, et al. Mutations of the microsomal triglyceride-transfer-protein gene in abetalipoproteinemia. Am J Hum Genet 1995; 57: 1298-1310.
30. Heath KE, Luong LA, Leonard JV, Chester A, Shoulders CC, Scott J, et al. The use of a highly informative CA repeat polymorphism within the abetalipoproteinaemia locus (4q22-24). Prenat Diagn 1997; 17: 1181-1186.
31. Yang XP, Inazu A, Yagi K, Kajinami K, Koizumi J, Mabuchi H. Abetalipoproteinemia caused by maternal isodisomy of chromosome 4q containing an intron 9 splice acceptor mutation in the microsomal triglyceride transfer protein gene. Arterioscler Thromb Vasc Biol 1999; 19: 1950-1955.
32. Ohashi K, Ishibashi S, Osuga J, Tozawa R, Harada K, Yahagi N, et al. Novel mutations in the microsomal triglyceride transfer protein gene causing abetalipoproteinemia. J Lipid Res 2000; 41: 1199-1204.
33. Wang J, Hegele RA. Microsomal triglyceride transfer protein (MTP) gene mutations in Canadian subjects with abetalipoproteinemia. Hum Mutat 2000; 15: 294-295.
34. Al-Shali K, Wang J, Rosen F, Hegele RA. Ileal adenocarcinoma in a mild phenotype of abetalipoproteinemia. Clin Genet 2003; 63: 135-138.
35. Berthier MT, Couture P, Houde A, Paradis AM, Sammak A, Verner A, et al. The c.419-420insA in the MTP gene is associated with abetalipoproteinemia among French-Canadians. Mol Genet Metab 2004; 81: 140-143.
36. Di Leo E, Lancellotti S, Penacchioni JY, Cefalu AB, Averna M, Pisciotta L, et al. Mutations in MTP gene in abeta- and hypobeta-lipoproteinemia. Atherosclerosis 2005; 180: 311-318.
37. Al-Mahdili HA, Hooper AJ, Sullivan DR, Stewart PM, Burnett JR. A mild case of abetalipoproteinaemia in association with subclinical hypothyroidism. Ann Clin Biochem 2006; 43: 516-519.
38. Sakamoto O, Abukawa D, Takeyama J, Arai N, Nagano M, Hattori H, et al. An atypical case of abetalipoproteinaemia with severe fatty liver in the absence of steatorrhoea or acanthocytosis. Eur J Pediatr 2006; 165: 68-70.
39. Benayoun L, Granot E, Rizel L, Allon-Shalev S, Behar DM, Ben-Yosef T. Abetalipoproteinemia in Israel: evidence for a founder mutation in the Ashkenazi Jewish population and a contiguous gene deletion in an Arab patient. Mol Genet Metab 2007; 90: 453-457.
40. Vongsuvanh R, Hooper AJ, Coakley JC, Macdessi JS, O'Loughlin EV, Burnett JR, et al. Novel mutations in abetalipoproteinaemia and homozygous familial hypobetalipoproteinaemia. J Inherit Metab Dis 2007; 30: 990.
41. Zamel R, Khan R, Pollex RL, Hegele RA. Abetalipoproteinemia: two case reports and literature review. Orphanet J Rare Dis 2008; 3: 19.
42. Najah M, Di Leo E, Awatef J, Magnolo L, Imene J, Pinotti E, et al. Identification of patients with abetalipoproteinemia and homozygous familial hypobetalipoproteinemia in Tunisia. Clin Chim Acta 2009; 401: 51-56.
43. Uslu N, Gurakan F, Yuce A, Demir H, Tarugi P. Abetalipoproteinemia in an infant with severe clinical phenotype and a novel mutation. Turk J Pediatr 2010; 52: 73-77.
44. Aminoff A, Gunnar E, Barbaro M, Mannila MN, Duponchel C, Tosi M, et al. Novel mutations in microsomal triglyceride transfer protein including maternal uniparental disomy in two patients with abetalipoproteinemia. Clin Genet 2011; 82: 197-200.
45. Pons V, Rolland C, Nauze M, Danjoux M, Gaibelet G, Durandy A, et al. A severe form of abetalipoproteinemia caused by new splicing mutations of microsomal triglyceride transfer protein (MTTP). Hum Mutat 2011; 32: 751-759.
46. Sani MN, Sabbaghian M, Mahjoob F, Cefalu AB, Averna MR, Rezaei N. Identification of a novel mutation of MTP gene in a patient with abetalipoproteinemia. Ann Hepatol 2011; 10: 221-226.
47. Khatun I, Walsh MT, Hussain MM. Loss of both phospholipid and triglyceride transfer activities of microsomal triglyceride transfer protein in abetalipoproteinemia. J Lipid Res 2013; 54: 1541-1549.
48. Magnolo L, Najah M, Fancello T, Di Leo E, Pinotti E, Brini I, et al. Novel mutations in SAR1B and MTTP genes in Tunisian children with chylomicron retention disease and abetalipoproteinemia. Gene 2013; 512: 28-34.
49. Mohamed N, Mohamed Youssef S, Mohamed Yahia H, Afef S, Awatef J, Saber H, et al. Molecular characterization of Tunisian families with abetalipoproteinemia and identification of a novel mutation in MTTP gene. Diagn Pathol 2013; 8: 54.
50. Yang CY, Kim TW, Weng SA, Lee BR, Yang ML, Gotto Jr AM. Isolation and characterization of sulfhydryl and disulfide peptides of human apolipoprotein B-100. Proc Natl Acad Sci U S A 1990; 87: 5523-5527.
51. Salt HB, Wolff OH, Lloyd JK, Fosbrooke AS, Cameron AH, Hubble DV. On having no beta-lipoprotein. A syndrome comprising a-beta-lipoproteinaemia, acanthocytosis, and steatorrhoea. Lancet 1960; 2: 325-329.
52. Biemer JJ, McCammon RE. The genetic relationship of abetalipoproteinemia and hypobetalipoproteinemia: a report of the occurrence of both diseases within the same family. J Lab Clin Med 1975; 85: 556-565.
53. Illingworth DR, Connor WE, Buist NR, Jhaveri BM, Lin DS, McMurry MP. Sterol balance in abetalipoproteinemia: studies in a patient with homozygous familial hypobetalipoproteinemia. Metabolism 1979; 28: 1152-1160.
54. Steinberg D, Grundy SM, Mok HY, Turner JD, Weinstein DB, Brown WV, et al. Metabolic studies in an unusual case of asymptomatic familial hypobetalipoproteinemia with hypoalphalipoproteinemia and fasting chylomicronemia. J Clin Invest 1979; 64: 292-301.
55. Malloy MJ, Kane JP, Hardman DA, Hamilton RL, Dalal KB. Normotriglyceridemic abetalipoproteinemia. Absence of the B-100 apolipoprotein. J Clin Invest 1981; 67: 1441-1450.
56. Berger GM, Brown G, Henderson HE, Bonnici F. Apolipoprotein B detected in the plasma of a patient with homozygous hypobetalipoproteinaemia: implications for aetiology. J Med Genet 1983; 20: 189-195.
57. Takashima Y, Kodama T, Iida H, Kawamura M, Aburatani H, Itakura H, et al. Normotriglyceridemic abetalipoproteinemia in infancy: an isolated apolipoprotein B-100 deficiency. Pediatrics 1985; 75: 541-546.
58. Young SG, Bertics SJ, Curtiss LK, Dubois BW, Witztum JL. Genetic analysis of a kindred with familial hypobetalipoproteinemia. Evidence for two separate gene defects: one associated with an abnormal apolipoprotein B species, apolipoprotein B-37; and a second associated with low plasma concentrations of apolipoprotein B-100. J Clin Invest 1987; 79: 1842-1851.
59. Young SG, Bertics SJ, Curtiss LK, Witztum JL. Characterization of an abnormal species of apolipoprotein B, apolipoprotein B-37, associated with familial hypobetalipoproteinemia. J Clin Invest 1987; 79: 1831-1841.
60. Young SG, Peralta FP, Dubois BW, Curtiss LK, Boyles JK, Witztum JL. Lipoprotein B37, a naturally occurring lipoprotein containing the aminoterminal portion of apolipoprotein B100, does not bind to the apolipoprotein B, E (low density lipoprotein) receptor. J Biol Chem 1987; 262: 16604-16611.
61. Collins DR, Knott TJ, Pease RJ, Powell LM, Wallis SC, Robertson S, et al. Truncated variants of apolipoprotein B cause hypobetalipoproteinaemia. Nucleic Acids Res 1988; 16: 8361-8375.
62. Ross RS, Gregg RE, Law SW, Monge JC, Grant SM, Higuchi K, et al. Homozygous hypobetalipoproteinemia: a disease distinct from abetalipoproproteinemia at the molecular level. J Clin Invest 1988; 81: 590-595.
63. Young SG, Northey ST, McCarthy BJ. Low plasma cholesterol levels caused by a short deletion in the apolipoprotein B gene. Science 1988; 241: 591-593.
64. Harano Y, Kojima H, Nakano T, Harada M, Kashiwagi A, Nakajima Y, et al. Homozygous hypobetalipoproteinemia with spared chylomicron formation. Metabolism 1989; 38: 1-7.
65. Huang LS, Ripps ME, Korman SH, Deckelbaum RJ, Breslow JL. Hypobetalipoproteinemia due to an apolipoprotein B gene exon 21 deletion derived by Alu-Alu recombination. J Biol Chem 1989; 264: 11394-11400.
66. Krul ES, Kinoshita M, Talmud P, Humphries SE, Turner S, Goldberg AC, et al. Two distinct truncated apolipoprotein B species in a kindred with hypobetalipoproteinemia. Arteriosclerosis 1989; 9: 856-868.
67. Talmud P, King-Underwood L, Krul E, Schonfeld G, Humphries S. The molecular basis of truncated forms of apolipoprotein B in a kindred with compound heterozygous hypobetalipoproteinemia. J Lipid Res 1989; 30: 1773-1779.
68. Gay G, Pessah M, Bouma ME, Roche JF, Aymard JP, Beucler I, et al. Familial hypobetalipoproteinemia. Familial study of 4 cases. Rev Med Interne 1990; 11: 273-279.
69. Tennyson GE, Gabelli C, Baggio G, Bilato C, Brewer Jr HB. Molecular defect in the apolipoprotein B gene in a patient with hypobetalipoproteinemia and three distinct ApoB species. Clin Res 1990; 38: 482.
70. Hardman DA, Pullinger CR, Hamilton RL, Kane JP, Malloy MJ. Molecular and metabolic basis for the metabolic disorder normotriglyceridemic abetalipoproteinemia. J Clin Invest 1991; 88: 1722-1729.
71. Huang LS, Kayden H, Sokol RJ, Breslow JL. ApoB gene nonsense and splicing mutations in a compound heterozygote for familial hypobetalipoproteinemia. J Lipid Res 1991; 32: 1341-1348.
72. Gabelli C. The lipoprotein metabolism of apolipoprotein B mutants. Curr Opin Lipidol 1992; 3: 208-214.
73. Linton MF, Pierotti V, Young SG. Reading-frame restoration with an apolipoprotein B gene frameshift mutation. Proc Natl Acad Sci U S A 1992; 89: 11431-11435.
74. Pullinger CR, Hillas E, Hardman DA, Chen GC, Naya-Vigne JM, Iwasa JA, et al. Two apolipoprotein B gene defects in a kindred with hypobetalipoproteinemia, one of which results in a truncated variant, apoB-61, in VLDL and LDL. J Lipid Res 1992; 33: 699-710.
75. Scoazec JY, Bouma ME, Roche JF, Blache D, Verthier N, Feldmann G, et al. Liver fibrosis in a patient with familial homozygous hypobetalipoproteinaemia: possible role of vitamin supplementation. Gut 1992; 33: 414-417.
76. Burnett JR, Proos AL, Koutts J, Burnett L. Familial hypobetalipoproteinaemia: a rare presentation to the lipid clinic. Med J Aust 1993; 159: 272-274.
77. Talmud PJ, Krul ES, Pessah M, Gay G, Schonfeld G, Humphries SE, et al. Donor splice mutation generates a lipid-associated apolipoprotein B-27.6 in a patient with homozygous hypobetalipoproteinemia. J Lipid Res 1994; 35: 468-477.
78. Young SG, Bihain B, Flynn LM, Sanan DA, Ayrault-Jarrier M, Jacotot B. Asymptomatic homozygous hypobetalipoproteinemia associated with apolipoprotein B45.2. Hum Mol Genet 1994; 3: 741-744.
79. Welty FK, Ordovas J, Schaefer EJ, Wilson PW, Young SG. Identification and molecular analysis of two apoB gene mutations causing low plasma cholesterol levels. Circulation 1995; 92: 2036-2040.
80. Gabelli C, Bilato C, Martini S, Tennyson GE, Zech LA, Corsini A, et al. Homozygous familial hypobetalipoproteinemia. Increased LDL catabolism in hypobetalipoproteinemia due to a truncated apolipoprotein B species, Apo B-87Padova. Arterioscler Thromb Vasc Biol 1996; 16: 1189-1196.
81. Ohashi K, Ishibashi S, Yamamoto M, Osuga J, Yazaki Y, Yukawa S, et al. A truncated species of apolipoprotein B (B-38.7) in a patient with homozygous hypobetalipoproteinemia associated with diabetes mellitus. Arterioscler Thromb Vasc Biol 1998; 18: 1330-1334.
82. Welty FK, Guida KA, Andersen JJ. Donor splice-site mutation (210+1G-C) in the ApoB gene causes a very low level of ApoB-100 and LDL cholesterol. Arterioscler Thromb Vasc Biol 2001; 21: 1864-1865.
83. Hegele RA, Miskie BA. Acanthocytosis in a patient with homozygous familial hypobetalipoproteinemia due to a novel APOB splice site mutation. Clin Genet 2002; 61: 101-103.
84. Burnett JR, Shan J, Miskie BA, Whitfield AJ, Yuan J, Tran K, et al. A novel nontruncating APOB gene mutation, R463W, causes familial hypobetalipoproteinemia. J Biol Chem 2003; 278: 13442-13452.
85. Whitfield AJ, Marais AD, Robertson K, Barrett PH, van Bockxmeer FM, Burnett JR. Four novel mutations in APOB causing heterozygous and homozygous familial hypobetalipoproteinemia. Hum Mutat 2003; 22: 178.
86. Fouchier SW, Sankatsing RR, Peter J, Castillo S, Pocovi M, Alonso R, et al. High frequency of APOB gene mutations causing familial hypobetalipoproteinaemia in patients of Dutch and Spanish descent. J Med Genet 2005; 42: e23.
87. Homer VM, George PM, du Toit S, Davidson JS, Wilson CJ. Mental retardation and ataxia due to normotriglyceridemic hypobetalipoproteinemia. Ann Neurol 2005; 58: 160-163.
88. Di Leo E, Magnolo L, Bertolotti M, Bourbon M, Carmo Pereira S, Pirisi M, et al. Variable phenotypic expression of homozygous familial hypobetalipoproteinaemia due to novel APOB gene mutations. Clin Genet 2008; 74: 267-273.
89. Katsuda S, Kawashiri MA, Inazu A, Tada H, Tsuchida M, Kaneko Y, et al. Apolipoprotein B gene mutations and fatty liver in Japanese hypobetalipoproteinemia. Clin Chim Acta 2009; 399: 64-68.
90. Gangloff A, Bergeron J, Couture P, Martins R, Hegele RA, Gagne C. A novel mutation of apolipoprotein B in a French Canadian family with homozygous hypobetalipoproteinemia. J Clin Lipidol 2011; 5: 414-417.
91. Partin JS, Partin JC, Schubert WK, McAdams AJ. Liver ultrastructure in abetalipoproteinemia: evolution of micronodular cirrhosis. Gastroenterology 1974; 67: 107-118.
92. Black DD, Hay RV, Rohwer-Nutter PL, Ellinas H, Stephens JK, Sherman H, et al. Intestinal and hepatic apolipoprotein B gene expression in abetalipoproteinemia. Gastroenterology 1991; 101: 520-528.
93. Braegger CP, Belli DC, Mentha G, Steinmann B. Persistence of the intestinal defect in abetalipoproteinaemia after liver transplantation. Eur J Pediatr 1998; 157: 576-578.
94. Lee J, Hegele RA. Abetalipoproteinemia and homozygous hypobetalipoproteinemia: a framework for diagnosis and management. J Inherit Metab Dis 2014; 37: 333-339.
95. Rubin D, Schneider-Muntau A, Klapper M, Nitz I, Helwig U, Folsch UR, et al. Functional analysis of promoter variants in the microsomal triglyceride transfer protein (MTTP) gene. Hum Mutat 2008; 29: 123-129.
96. Peng XE, Wu YL, Lu QQ, Hu ZJ, Lin X. MTTP polymorphisms and susceptibility to non-alcoholic fatty liver disease in a Han Chinese population. Liver Int 2014; 34: 118-128.
97. Lonardo A, Tarugi P, Ballarini G, Bagni A. Familial heterozygous hypobetalipoproteinemia, extrahepatic primary malignancy, and hepatocellular carcinoma. Dig Dis Sci 1998; 43: 2489-2492.
98. Heeks LV, Hooper AJ, Adams LA, Robbins P, Barrett PH, van Bockxmeer FM, et al. Non-alcoholic steatohepatitis-related cirrhosis in a patient with APOB L343V familial hypobetalipoproteinaemia. Clin Chim Acta 2013; 421: 121-125.
99. Durrington PN, Charlton-Menys V, Packard CJ, Caslake MJ, Wang J, Bhatnagar D, et al. Familial hypobetalipoproteinemia due to a novel early stop mutation. J Clin Lipidol 2008; 2: 384-390.
100. Bonnefont-Rousselot D, Condat B, Sassolas A, Chebel S, Bittar R, Federspiel MC, et al. Cryptogenic cirrhosis in a patient with familial hypocholesterolemia due to a new truncated form of apolipoprotein B. Eur J Gastroenterol Hepatol 2009; 21: 104-108.
101. Liao W, Hui TY, Young SG, Davis RA. Blocking microsomal triglyceride transfer protein interferes with apoB secretion without causing retention or stress in the ER. J Lipid Res 2003; 44: 978-985.
102. Hernandez-Gea V, Ghiassi-Nejad Z, Rozenfeld R, Gordon R, Fiel MI, Yue Z, et al. Autophagy releases lipid that promotes fibrogenesis by activated hepatic stellate cells in mice and in human tissues. Gastroenterology 2012; 142: 938-946.
103. Lee JS, Zheng Z, Mendez R, Ha SW, Xie Y, Zhang K. Pharmacologic ER stress induces non-alcoholic steatohepatitis in an animal model. Toxicol Lett 2012; 211: 29-38.
104. Zhong S, Magnolo AL, Sundaram M, Zhou H, Yao EF, Di Leo E, et al. Nonsynonymous mutations within APOB in human familial hypobetalipoproteinemia: evidence for feedback inhibition of lipogenesis and postendoplasmic reticulum degradation of apolipoprotein B. J Biol Chem 2010; 285: 6453-6464.
105. Dullaart RP, Speelberg B, Schuurman HJ, Milne RW, Havekes LM, Marcel YL, et al. Epitopes of apolipoprotein B-100 and B-48 in both liver and intestine. Expression and evidence for local synthesis in recessive abetalipoproteinemia. J Clin Invest 1986; 78: 1397-1404.
106. Anstee QM, Targher G, Day CP. Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nat Rev Gastroenterol Hepatol 2013; 10: 330-344.
107. Singal AG, Manjunath H, Yopp AC, Beg MS, Marrero JA, Gopal P, et al. The effect of PNPLA3 on fibrosis progression and development of hepatocellular carcinoma: a meta-analysis. Am J Gastroenterol 2014; 109: 325-334.
108. Berriot-Varoqueaux N, Aggerbeck LP, Samson-Bouma M, Wetterau JR. The role of the microsomal triglygeride transfer protein in abetalipoproteinemia. Annu Rev Nutr 2000; 20: 663-697.
109. Burnett JR, Bell DA, Hooper AJ, Hegele RA. Clinical utility gene card for: abetalipoproteinaemia. Eur J Hum Genet 2012; 20. http://dx.doi.org/10.1038/ejhg.2012.30.
110. Burnett JR, Bell DA, Hooper AJ, Hegele RA. Clinical utility gene card for: familial hypobetalipoproteinaemia (APOB). Eur J Hum Genet 2012; 20. http://dx.doi.org/10.1038/ejhg.2012.85.
111. Tarugi P, Lonardo A. Heterozygous familial hypobetalipoproteinemia associated with fatty liver. Am J Gastroenterol 1997; 92: 1400-1402.