A potential screening factor for accumulation of cholesteyl ester transfer protein deficiency in East Asia: Schistosoma japonicum

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 4, 2014, Pages 495-504

  Yokoyama, Shinji ^a  

^a CHUBU UNIVERSITY   (Japan)

Author keywords

CETP; CETP deficiency; Egg embryonation; HDL; Liver; Schistosoma

Indexed keywords

AMINO ACID; CD36 RELATED PROTEIN; CHOLESTEROL ESTER TRANSFER PROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LIPOPROTEIN RECEPTOR; PROTEIN; UNCLASSIFIED DRUG; CD36 ANTIGEN; CETP PROTEIN, HUMAN; CHOLESTEROL ESTER; HIGH DENSITY LIPOPROTEIN;

ARTICLE; CHOLESTEROL ESTER TRANSFER PROTEIN DEFICIENCY; CLONING; DISORDERS OF LIPID AND LIPOPROTEIN METABOLISM; ENDEMIC SPECIES; FRESHWATER ENVIRONMENT; GEOGRAPHIC DISTRIBUTION; HOST; HUMAN; IN VIVO STUDY; LIFE CYCLE STAGE; LIVER CIRRHOSIS; LIVER GRANULOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; SCHISTOSOMA JAPONICUM; SCHISTOSOMIASIS; SCHISTOSOMIASIS JAPONICA; SOUTHEAST ASIA; ANIMAL; ASIA; BLOOD; DEFICIENCY; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIVER; METABOLISM; MOUSE; OOCYTE; PARASITOLOGY; PATHOGENICITY; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD36; ASIA; CHOLESTEROL ESTER TRANSFER PROTEINS; CHOLESTEROL ESTERS; HUMANS; LIPID METABOLISM, INBORN ERRORS; LIPOPROTEINS, HDL; LIVER; MICE; MICE, TRANSGENIC; OVUM; SCHISTOSOMA JAPONICUM; SCHISTOSOMIASIS JAPONICA;

EID: 84896857087     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.12.014     Document Type: Review

References (72)

1. D. Drayna, A.S. Jarnagin, J. McLean, W. Henzel, W. Kohr, C. Fielding, and R. Lawn Cloning and sequencing of human cholesteryl ester transfer protein cDNA Nature 327 1987 632 634 (Pubitemid 17086900)
2. K.W. Ko, T. Ohnishi, and S. Yokoyama Triglyceride transfer is required for net cholesteryl ester transfer between lipoproteins in plasma by lipid transfer protein. Evidence for a hetero-exchange transfer mechanism demonstrated by using novel monoclonal antibodies J. Biol. Chem. 269 1994 28206 28213
3. T. Ohnishi, C. Tan, and S. Yokoyama Selective transfer of cholesteryl ester over triglyceride by human plasma lipid transfer protein between apolipoprotein-activated lipid microemulsion Biochemistry 33 1994 4533 4542 (Pubitemid 24145101)
4. X. Qiu, A. Mistry, M.J. Ammirati, B.A. Chrunyk, R.W. Clark, Y. Cong, J.S. Culp, D.E. Danley, T.B. Freeman, K.F. Geoghegan, M.C. Griffor, S.J. Hawrylik, C.M. Hayward, P. Hensley, L.R. Hoth, G.A. Karam, M.E. Lira, D.B. Lloyd, K.M. McGrath, K.J. Stutzman-Engwall, A.K. Subashi, T.A. Subashi, J.F. Thompson, I.K. Wang, H. Zhao, and A.P. Seddon Crystal structure of cholesteryl ester transfer protein reveals a long tunnel and four bound lipid molecules Nat. Struct. Mol. Biol. 14 2007 106 113
5. A. Tall Plasma lipid transfer proteins Annu. Rev. Biochem. 64 1995 235 257
6. B. Foger, A. Ritsch, A. Doblinger, H. Wessels, and J.R. Patsch Relationship of plasma cholesteryl ester transfer protein to HDL cholesterol. Studies in normotriglyceridemia and moderate hypertriglyceridemia Arterioscler. Thromb. Vasc. Biol. 16 1996 1430 1436 (Pubitemid 26427595)
7. H. Czarnecka, and S. Yokoyama Regulation of cellular cholesterol efflux by lecithin:cholesterol acyltransferase reaction through nonspecific lipid exchange J. Biol. Chem. 271 1996 2023 2028 (Pubitemid 26047786)
8. T. Kurasawa, S. Yokoyama, Y. Miyake, T. Yamamura, and S. Yokoyama Rate of cholesteryl ester transfer between high and low density lipoproteins in human serum and a case with decreased transfer rate in association with hyperalphalipoproteinemia J. Biochem. 98 1985 1499 1508 (Pubitemid 16169184)
9. J. Koizumi, H. Mabuchi, A. Yoshimura, I. Michishita, M. Takeda, H. Itoh, Y. Sakai, T. Sakai, K. Ueda, and R. Takeda Deficiency of serum cholesteryl-ester transfer activity in patients with familial hyperalphalipoproteinaemia Atherosclerosis 58 1985 175 186 (Pubitemid 16173307)
10. M.L. Brown, A. Inazu, C.B. Hesler, L.B. Agellon, C. Mann, M.E. Whitlock, Y.L. Marcel, R.W. Milne, J. Koizumi, and H. Mabuchi et al. Molecular basis of lipid transfer protein deficiency in a family with increased high-density lipoproteins Nature 342 1989 448 451 (Pubitemid 19277523)
11. A. Inazu, X.C. Jiang, T. Haraki, K. Yagi, N. Kamon, J. Koizumi, H. Mabuchi, R. Takeda, K. Takata, and Y. Moriyama et al. Genetic cholesteryl ester transfer protein deficiency caused by two prevalent mutations as a major determinant of increased levels of high density lipoprotein cholesterol J. Clin. Invest. 94 1994 1872 1882 (Pubitemid 24348224)
12. N. Sakai, S. Yamashita, K. Hirano, M. Menju, T. Arai, K. Kobayashi, M. Ishigami, Y. Yoshida, T. Hoshino, and N. Nakajima et al. Frequency of exon 15 missense mutation (442D:G) in cholesteryl ester transfer protein gene in hyperalphalipoproteinemic Japanese subjects Atherosclerosis 114 1995 139 145
13. K. Hirano, S. Yamashita, N. Nakajima, T. Arai, T. Maruyama, Y. Yoshida, M. Ishigami, N. Sakai, K. Kameda-Takemura, and Y. Matsuzawa Genetic cholesteryl ester transfer protein deficiency is extremely frequent in the Omagari area of Japan. Marked hyperalphalipoproteinemia caused by CETP gene mutation is not associated with longevity. Arterioscler. Thromb. Vasc. Biol. 17 1997 1053 1059 (Pubitemid 27260323)
14. T. Maruyama, S. Yamashita, Y. Matsuzawa, H. Bujo, K. Takahashi, Y. Saito, S. Ishibashi, K. Ohashi, F. Shionoiri, T. Gotoda, N. Yamada, and T. Kita Mutations in Japanese subjects with primary hyperlipidemia - results from the Research Committee of the Ministry of Health and Welfare of Japan since 1996 J. Atheroscler. Thromb. 11 2004 131 145
15. S. Yamashita, K. Hirano, N. Sakai, and Y. Matsuzawa Molecular biology and pathophysiological aspects of plasma cholesteryl ester transfer protein Biochim. Biophys. Acta 1529 2000 257 275
16. M. Nagano, S. Yamashita, K. Hirano, M. Takano, T. Maruyama, M. Ishihara, Y. Sagehashi, T. Kujiraoka, K. Tanaka, H. Hattori, N. Sakai, N. Nakajima, T. Egashira, and Y. Matsuzawa Molecular mechanisms of cholesteryl ester transfer protein deficiency in Japanese J. Atheroscler. Thromb. 11 2004 110 121
17. A. Ritsch, H. Drexel, F.W. Amann, C. Pfeifhofer, and J.R. Patsch Deficiency of cholesteryl ester transfer protein: description of molecular defect and the dissociation of cholesteryl ester and triglyceride transfer in plasma Arterioscler. Thromb. Vasc. Biol. 17 1997 3433 3441 (Pubitemid 28028553)
18. S.-P. Hui Frequency and effect on plasma lipoprotein metabolism of a mutation in the cholesteryl ester transfer protein gene in the Chinese Hokkaido J. Med. Sci. 72 1997 319 327
19. D.W. Chen, J.F. Yang, Z. Tang, X.M. Dong, X.L. Feng, S. Yu, and P. Chan Cholesteryl ester transfer protein polymorphism D442G associated with a potential decreased risk for Alzheimer's disease as a modifier for APOE epsilon4 in Chinese Brain Res. 1187 2008 52 57 (Pubitemid 350191809)
20. T.S. Jap, Y.C. Wu, Y.C. Tso, and C.Y. Chiu A novel mutation in the intron 1 splice donor site of the cholesterol ester transfer protein (CETP) gene as a cause of hyperalphalipoproteinemia Metabolism 51 2002 394 397
21. L.A. Hsu, Y.L. Ko, K.H. Hsu, Y.H. Ko, and Y.S. Lee Genetic variations in the cholesteryl ester transfer protein gene and high density lipoprotein cholesterol levels in Taiwanese Chinese Hum. Genet. 110 2002 57 63
22. G.-J. Song, G.-H. Han, J.-J. Chae, Y. Namkoong, H.-K. Lee, Y.-B. Park, and C.-C. Lee The effect of the cholesterol ester transfer protein gene and environmental factors on the plasma high density lipoprotein cholesterol levels in the Korean population Mol. Cells 7 1997 615 619 (Pubitemid 127477544)
23. W. Plengpanich, S. Siriwong, and W. Khovidhunkit Two novel mutations and functional analyses of the CETP and LIPC genes underlying severe hyperalphalipoproteinemia Metabolism 58 2009 1178 1184
24. M. Nagano, S. Yamashita, K. Hirano, M. Ito, T. Maruyama, M. Ishihara, Y. Sagehashi, T. Oka, T. Kujiraoka, H. Hattori, N. Nakajima, T. Egashira, M. Kondo, N. Sakai, and Y. Matsuzawa Two novel missense mutations in the CETP gene in Japanese hyperalphalipoproteinemic subjects: high-throughput assay by Invader assay J. Lipid Res. 43 2002 1011 1018 (Pubitemid 34760871)
25. Y.Q. Ma, G.N. Thomas, J.A. Critchley, J.C. Chan, Z.S. Lee, and B. Tomlinson Identification of the intron 14 splicing defect of the cholesteryl ester transfer protein gene in Hong Kong Chinese Clin. Genet. 59 2001 287 289 (Pubitemid 32318398)
26. E.M. Teh, P.J. Dolphin, W.C. Breckenridge, and M.H. Tan Human plasma CETP deficiency: identification of a novel mutation in exon 9 of the CETP gene in a Caucasian subject from North America J. Lipid Res. 39 1998 442 456 (Pubitemid 28100681)
27. S.A. Hill, D.J. Nazir, P. Jayaratne, K.S. Bamford, and M.J. McQueen Mutations in cholesteryl ester transfer protein and hepatic lipase in a North American population Clin. Biochem. 30 1997 413 418 (Pubitemid 27329349)
28. W.A. van der Steeg, G.K. Hovingh, A.H. Klerkx, B.A. Hutten, I.C. Nootenboom, J.H. Levels, A. van Tol, G.M. Dallinga-Thie, A.H. Zwinderman, J.J. Kastelein, and J.A. Kuivenhoven Cholesteryl ester transfer protein and hyperalphalipoproteinemia in Caucasians J. Lipid Res. 48 2007 674 682 (Pubitemid 46397470)
29. J. Rhyne, M.J. Ryan, C. White, T. Chimonas, and M. Miller The two novel CETP mutations Gln87X and Gln165X in a compound heterozygous state are associated with marked hyperalphalipoproteinemia and absence of significant coronary artery disease J. Mol. Med. (Berl) 84 2006 647 650 (Pubitemid 44162554)
30. A.B. Cefalu, D. Noto, L. Magnolo, E. Pinotti, M. Gomaraschi, S. Martini, G.B. Vigna, L. Calabresi, P. Tarugi, and M.R. Averna Novel mutations of CETP gene in Italian subjects with hyperalphalipoproteinemia Atherosclerosis 204 2009 202 207
31. L. Calabresi, P. Nilsson, E. Pinotti, M. Gomaraschi, E. Favari, M.P. Adorni, F. Bernini, C.R. Sirtori, S. Calandra, G. Franceschini, and P. Tarugi A novel homozygous mutation in CETP gene as a cause of CETP deficiency in a Caucasian kindred Atherosclerosis 205 2009 506 511
32. S. Chantepie, A.E. Bochem, M.J. Chapman, G.K. Hovingh, and A. Kontush High-density lipoprotein (HDL) particle subpopulations in heterozygous cholesteryl ester transfer protein (CETP) deficiency: maintenance of antioxidative activity PLoS One 7 2012 e49336
33. A. Thompson, E. Di Angelantonio, N. Sarwar, S. Erqou, D. Saleheen, R.P. Dullaart, B. Keavney, Z. Ye, and J. Danesh Association of cholesteryl ester transfer protein genotypes with CETP mass and activity, lipid levels, and coronary risk JAMA 299 2008 2777 2788 (Pubitemid 351846853)
34. A. Inazu, M.L. Brown, C.B. Hesler, L.B. Agellon, J. Koizumi, K. Takata, Y. Maruhama, H. Mabuchi, and A.R. Tall Increased high-density lipoprotein levels caused by a common cholesteryl-ester transfer protein gene mutation N. Engl. J. Med. 323 1990 1234 1238 (Pubitemid 20366528)
35. S. Yamashita, D.L. Sprecher, N. Sakai, Y. Matsuzawa, S. Tarui, and D.Y. Hui Accumulation of apolipoprotein E-rich high density lipoproteins in hyperalphalipoproteinemic human subjects with plasma cholesteryl ester transfer protein deficiency J. Clin. Invest. 86 1990 688 695 (Pubitemid 20327355)
36. S. Yamashita, D.Y. Hui, J.R. Wetterau, D.L. Sprecher, J.A.K. Harmony, N. Sakai, Y. Matsuzawa, and S. Tarui Characterization of plasma lipoproteins in patients heterozygous for human plasma cholesteryl ester transfer protein (CETP) deficeiency: plasma CETP regulated high-density lipoprotein concentration and composition Metabolism 40 1991 756 763
37. N. Sakai, Y. Matsuzawa, K. Hirano, S. Yamashita, S. Nozaki, Y. Ueyama, M. Kubo, and S. Tarui Detection of two species of low density lipoprotein particles in cholesteryl ester transfer protein deficiency Arterioscler. Thromb. 11 1991 71 79
38. C.L. Bisgaier, M.V. Siebenkas, M.L. Brown, A. Inazu, J. Koizumi, H. Mabuchi, and A.R. Tall Familial cholesteryl ester transfer protein deficiency is associated with triglyceride-rich low density lipoproteins containing cholesteryl esters of probable intracellular origin J. Lipid Res. 32 1991 21 33
39. Y. Moriyama, T. Okamura, A. Inazu, M. Doi, H. Iso, Y. Mouri, Y. Ishikawa, H. Suzuki, M. Iida, J. Koizumi, H. Mabuchi, and Y. Komachi A low prevalence of coronary heart disease among subjects with increased high-density lipoprotein cholesterol levels, including those with plasma cholesteryl ester transfer protein deficiency Prev. Med. 27 1998 659 667 (Pubitemid 28452494)
40. J.D. Curb, R.D. Abbott, B.L. Rodriguez, K. Masaki, R. Chen, D.S. Sharp, and A.R. Tall A prospective study of HDL-C and cholesteryl ester transfer protein gene mutations and the risk of coronary heart disease in the elderly J. Lipid Res. 45 2004 948 953 (Pubitemid 38552866)
41. S.E. Nissen, J.C. Tardif, S.J. Nicholls, J.H. Revkin, C.L. Shear, W.T. Duggan, W. Ruzyllo, W.B. Bachinsky, G.P. Lasala, and E.M. Tuzcu Effect of torcetrapib on the progression of coronary atherosclerosis N. Engl. J. Med. 356 2007 1304 1316 (Pubitemid 46513296)
42. G.G. Schwartz, A.G. Olsson, M. Abt, C.M. Ballantyne, P.J. Barter, J. Brumm, B.R. Chaitman, I.M. Holme, D. Kallend, L.A. Leiter, E. Leitersdorf, J.J. McMurray, H. Mundl, S.J. Nicholls, P.K. Shah, J.C. Tardif, and R.S. Wright Effects of dalcetrapib in patients with a recent acute coronary syndrome N. Engl. J. Med. 367 2012 2089 2099
43. C. Betard, A.M. Kessling, M. Roy, A. Chamberland, S. Lussier-Cacan, and J. Davignon Molecular genetic evidence for a founder effect in familial hypercholesterolemia among French Canadians Hum. Genet. 88 1992 529 536
44. M. Torrington, J.L. Botha, G.J. Pilcher, and S.G. Baker Association between familial hypercholesterolaemia and church affiliation. Is this the result of sociocultural isolation of migrant farmers in 19th-century South Africa? S. Afr. Med. J. 65 1984 762 767 (Pubitemid 14119348)
45. M. Abifadel, J.P. Rabes, S. Jambart, G. Halaby, M.H. Gannage-Yared, A. Sarkis, G. Beaino, M. Varret, N. Salem, S. Corbani, H. Aydenian, C. Junien, A. Munnich, and C. Boileau The molecular basis of familial hypercholesterolemia in Lebanon: spectrum of LDLR mutations and role of PCSK9 as a modifier gene Hum. Mutat. 30 2009 E682 E691
46. A.C. Allison Protection afforded by sickle-cell trait against subtertian malareal infection Br. Med. J. 1 1954 290 294
47. P.W. Hedrick Resistance to malaria in humans: the impact of strong, recent selection Malar. J. 11 2012 349
48. S.M. Taylor, C.M. Parobek, and R.M. Fairhurst Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis Lancet Infect. Dis. 12 2012 457 468
49. F.D. Rumjanek, E.G. Campos, and L.C. Afonso Evidence for the occurrence of LDL receptors in extracts of schistosomula of Schistosoma mansoni Mol. Biochem. Parasitol. 28 1988 145 152 (Pubitemid 18078182)
50. F.D. Rumjanek, D.J. McLaren, and S.R. Smithers Serum-induced expression of a surface protein in schistosomula of Schistosoma mansoni: a possible receptor for lipid uptake Mol. Biochem. Parasitol. 9 1983 337 350 (Pubitemid 14200252)
51. X. Xu, and J.P. Caulfield Characterization of human low density lipoprotein binding proteins on the surface of Schistosomula of Schistosoma mansoni Eur. J. Cell Biol. 57 1992 229 235
52. S.T. Furlong, K.S. Thibault, L.M. Morbelli, J.J. Guinn, and R.A. Rogers Uptake and compartmentalization of fluorescent lipid analogs in larval Schistosoma mansoni J. Lipid Res. 36 1995 1 12
53. M.V. Rogers, D. Quilici, G.F. Mitchell, and N.H. Fidge Purification of a putative lipoprotein receptor from Schistosoma japonicum adult worms Mol. Biochem. Parasitol. 41 1990 93 100 (Pubitemid 20176672)
54. J. Fan, G. Xiaoxian, W. Yang, L. Shen, D.P. McManus, and P.J. Brindley A Schistosoma japonicum very low-density lipoprotein-binding protein Int. J. Biochem. Cell Biol. 1507 2003 1 16
55. D.P. McManus, D.J. Gray, Y. Li, Z. Feng, G.M. Williams, D. Stewart, J. Rey-Ladino, and A.G. Ross Schistosomiasis in the People's Republic of China: the era of the Three Gorges Dam Clin. Microbiol. Rev. 23 2010 442 466
56. L.D. Wang, H.G. Chen, J.G. Guo, X.J. Zeng, X.L. Hong, J.J. Xiong, X.H. Wu, X.H. Wang, L.Y. Wang, G. Xia, Y. Hao, D.P. Chin, and X.N. Zhou A strategy to control transmission of Schistosoma japonicum in China N. Engl. J. Med. 360 2009 121 128
57. R. Bergquist, and M. Tanner Controlling schistosomiasis in Southeast Asia: a tale of two countries Adv. Parasitol. 72 2010 109 144
58. C.A. Gordon, L.P. Acosta, D.J. Gray, R.M. Olveda, B. Jarilla, G.N. Gobert, A.G. Ross, and D.P. McManus High prevalence of Schistosoma japonicum infection in Carabao from Samar Province, the Philippines: implications for transmission and control PLoS Negl. Trop. Dis. 6 2012 e1778
59. C. Harinasuta Epidemiology and control of schistosomiasis in Southeast Asia Southeast Asian J. Trop. Med. Public Health 15 1984 431 438 (Pubitemid 15077032)
60. F. Iida, R. Iida, H. Kamijo, K. Takaso, Y. Miyazaki, W. Funabashi, K. Tsuchiya, and Y. Matsumoto Chronic Japanese schistosomiasis and hepatocellular carcinoma: ten years of follow-up in Yamanashi Prefecture, Japan Bull. World Health Organ. 77 1999 573 581 (Pubitemid 29352538)
61. A.G.P. Ross, P.B. Bartley, A.C. Sleigh, G.R. Olds, Y. Li, G.M. Williams, and D.P. McManus Schistosomiasis N. Engl. J. Med. 346 2002 1212 1220 (Pubitemid 34984584)
62. J. Mohda, C.A. Redman, J.A. Thormhill, and J.R. Kusel Schistosomes: unanswered questions on the basic biology of the host-parasite relationship Prasitol. Today 14 1998 396 401 (Pubitemid 28511201)
63. M. Hirata, M. Takushima, M. Kaga, and T. Fukuma Induction of experimental murine granuloma formation against Schistosoma japonicum eggs produced by in vitro ova deposition, in vitro tissue extraction, or lyophilization Parasitol. Res. 77 1991 315 319
64. R. El Ridi, P. Velupillai, and D.A. Harn Regulation of Schistosome egg granuloma formation: host-soluble l-selectin enters tissue-trapped eggs and binds to carbohydrate antigens on surface membrane of miracidia Infect. Immun. 64 1996 4700 4705 (Pubitemid 26357080)
65. G. Mitchell, E.G. Garcia, P.T. Rivera, W.U. Tiu, and K.M. Davern Evidence for and implications of anti-embryonation immunity in Schistosomiasis Exp. Parasitol. 79 1994 546 549
66. K. Okumura-Noji, Y. Miura, R. Lu, K. Asai, N. Ohta, P.J. Brindley, and S. Yokoyama CD36-related protein in Schistosoma japonicum: candidate mediator of selective cholesteryl ester uptake from high-density lipoprotein for egg maturation FASEB J. 27 2013 1236 1244
67. K. Okumura-Noji, K. Sasai, R. Zhan, H. Kawaguchi, H. Maruyama, T. Tada, H. Takahashi, M. Okazaki, T. Miida, N. Sakuma, G. Kimura, N. Ohta, and S. Yokoyama Cholesteryl ester transfer protein deficiency causes slow egg embryonation of Schistosoma japonicum Biochem. Biophys. Res. Commun. 286 2001 305 310 (Pubitemid 32924913)
68. S. Acton, A. Gigotti, T. Landschulz, S. Xu, H.H. Hobbs, and M. Krieger Identification of scavenger receptor SR-BI as a high density lipoprotein receptor Science 271 1996 518 520
69. K. Murao, V. Terpstra, S.R. Green, N. Kondratenko, D. Steinberg, and O. Quehenberger Characterization of CLA-1, a human homologue of rodent scavenger receptor BI, as a receptor for high density lipoprotein and apoptotic thymocytes J. Biol. Chem. 272 1997 17551 17557 (Pubitemid 27311188)
70. S. Yang, P.J. Brindley, Q. Zeng, Y. Li, J. Zhou, Y. Liu, B. Liu, L. Cai, T. Zeng, Q. Wei, L. Lan, and D.P. McManus Transduction of Schistosoma japonicum schistosomules with vesicular stomatitis virus glycoprotein pseudotyped murine leukemia retrovirus and expression of reporter human telomerase reverse transcriptase in the transgenic schistosomes Mol. Biochem. Parasitol. 174 2010 109 116
71. G. Rinaldi, S.E. Eckert, I.J. Tsai, S. Suttiprapa, K.J. Kines, J.F. Tort, V.H. Mann, D.J. Turner, M. Berriman, and P.J. Brindley Germline transgenesis and insertional mutagenesis in Schistosoma mansoni mediated by murine leukemia virus PLoS Pathog. 8 2012 e1002820
72. H. Shao, X. Li, T.J. Nolan, H.C. Massey, E.J. Pearce, and J.B. Lok Transposon-mediated chromosomal integration of transgenes in the parasitic nematode strongyloides ratti and establishment of stable transgenic lines PLoS Pathog. 8 2012 e1002871