An unusual host-parasite relationship: The growth hormone-like factor from plerocercoids of spirometrid tapeworms

International Journal for Parasitology

Volumn 26, Issue 6, 1996, Pages 575-588

  Phares, Kirk ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Cysteine proteinase; Growth hormone; Growth hormone receptor; Host parasite relationships; Plerocercoid growth factor; Spirometra mansonoides; Tapeworm growth factor

Indexed keywords

CYSTEINE PROTEINASE; GROWTH FACTOR; GROWTH HORMONE; GROWTH HORMONE RECEPTOR;

CESTODE; HOST PARASITE INTERACTION; LARVA; NONHUMAN; REVIEW;

CESTODA; MAMMALIA; PSEUDOPHYLLIDEA; SPIROMETRA MANSONOIDES;

GROWTH FACTOR; HOST-PARASITE RELATIONSHIP; TAPEWORM;

EID: 0030153360     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/0020-7519(96)00025-2     Document Type: Review

References (79)

1. Chang T. W., Raben M. S., Mueller J. F. & Weinstein L. 1973. Cultivation of the sparganum of Spirometra mansonoides in vitro with prolonged production of sparganum growth factor. Proceedings of the Society for Experimental Biology and Medicine 143: 134-144.
2. Corkum K. C. 1966. Sparganosis in some vertebrates of Louisiana and observations on a human infection. Journal of Parasitology 52: 444-448.
3. Cunningham B. C., Ultsch M., de Vos A. M., Mulkerrin M. G., Clauser K. R. & Wells J. A. 1991. Dimerization of the extracellular domain of the human growth hormone receptor by a single hormone molecule. Science 254: 821-825.
4. de Vos A. M., Ultsch M. & Kossiakoff A. A. 1992. Human growth hormone and the extracellular domain of its receptor: crystal structure of the complex. Science 255: 306-312.
5. Doenhoff M. J., Curtis R. H. C., Ngaiza J. & Modha J. 1990. Proteases in the schistosome life cycle: a paradigm for tumor metastasis. Cancer and Metastasis Reviews 9: 381-392.
6. Fukumoto S., Takafumi T., Hirai K. & Phares C. K. 1992. Comparison of isoenzyme patterns between Spirometra erinacei and Spirometra mansonoides by isoelectric focusing. Journal of Parasitology 78(4): 735-738.
7. Gala R. R. 1991. Prolactin and growth hormone in the regulation of the immune system. Proceedings of the Society for Experimental Biology and Medicine 198: 513-527.
8. Garland J. T., Ruegamer W. R. & Daughaday W. H. 1971. Induction of sulfation factor activity by infection of hypophysectomised rats with Spirometra mansonoides. Endocrinology 88: 924-927.
9. Garland J. T. & Daughaday W. H. 1972. Feedback inhibition of pituitary growth hormone in rats infected with Spirometra mansonoides. Proceedings of the Society for Experimental Biology and Medicine 139: 497-499.
10. Glitzer M. S. & Steelman S. L. 1971. The effect of the implantation of Spirometra mansonoides spargana in the growing rat. Proceedings of the Society for Experimental Biology and Medicine 138: 610-613.
11. Harlow D. R., Mertz W. & Mueller J. F. 1967. Insulin-like activity from the sparganum of Spirometra mansonoides. Journal of Parasitology 53: 449-454.
12. Hill R. E. & Hastie N. D. 1987. Accelerated evolution in the reactive centre regions of serine protease inhibitors. Nature London 326: 96-99.
13. Hirai K., Nishida H. & Shiwaku K. 1978. Studies on the plerocercoid growth factor of Spirometra erinacei (Rudolphi, 1819) with special reference to the effect on lipid mobilization in vitro. Japanese Journal of Parasitology 27: 527-533.
14. Hirai K., Shiwaku K., Tsuboi T., Torii M., Nishida H. & Yamane Y. 1983. Biological effects of Spirometra erinacei plerocercoids in several species of rodents. Zeitschrift für Parasitenkunde 69: 489-499.
15. Hirai K., Tsuboi T. & Torii M. 1986. Purification of the growth hormone-like substance from the plerocercoid of Spirometra erinacei. Japanese Journal of Parasitology 35suppl: 106.
16. Hirai K., Tsuboi T., Torii M. & Nishida H. 1987. Carbohydrate metabolism in intact golden hamsters infected with plerocercoids of Spirometra erinacei (Cestoda: Diphyllobothriidae). Parasitology Research 74: 183-187.
17. Hirai K., Shiwaku K., Tsuboi T., Torii M., Nishida H., Saheki S. & Kuno T. 1990. Hepatocyte growth factor produced by the plerocercoid of Spirometra erinacei. Ehime Medical Journal 9: 525-532.
18. Isaksson O. G. P., Edén S., Albertsson-Wikland K., Jansson J.-O., Friberg U. & Madsen K. 1986. Direct action of growth hormone on cartilage growth. In: Human Growth Hormone (Edited by Raiti S. & Tolman R. A.), pp. 563-573. Plenum, New York.
19. Kelly P. A., Postel-Vinay M. C., Finidori J., Edery M., Sotiropoulos A., Goujon L. & Esposito N. 1994. Growth hormone receptor structure, dimerization and function. Acta Paediatric Supplement 399: 107-111.
20. Kong Y., Chung Y.-B., Cho S.-Y. & Kang S.-Y. 1994. Cleavage of immunoglobulin G by excretory-secretory cathepsin S-like protease of Spirometra mansoni plerocercoid. Parasitology 109: 611-621.
21. Kostyo J. L. 1986. The multivalent nature of growth hormone. In: Human Growth Hormone (Edited by Raiti G. & Tolman R.), pp. 449-453. Plenum, New York.
22. Lesniak M., Roth J., Gordon P. & Gavin J. R., III. 1973. Human growth hormone radioreceptor assay using cultured human lymphocytes. Nature, New Biology 241: 20-22. .
23. Mueller J. F. 1935. A Diphyllobothrium from cats and dogs in the Syracuse region. Journal of Parasitology 21: 114-121.
24. Mueller J. F. 1937. A repartition of the genus Diphyllobothrium. Journal of Parasitology 23: 308-310.
25. Mueller J. F. & Coulston F. 1941. Experimental human infection with the sparganum larva of Spirometra mansonoides (Mueller, 1935). American Journal of Tropical Medicine 21: 399-425.
26. Mueller J. F. 1959. The laboratory propagation of Spirometra mansonoides as an experimental tool. I. Collecting, incubation and hatching of the eggs. Journal of Parasitology 45: 353-361.
27. Mueller J. F. 1959. The laboratory propagation of Spirometra mansonoides as an experimental tool. II. Culture and infection of the copepod host, and harvesting the procercoid. Transactions of the American Microbiological Society 78: 245-255.
28. Mueller J. F. 1963. Parasite-induced weight gain in mice. Annals of the New York Academic Science 113: 217-233.
29. Mueller J. F. 1965. Further studies on parasitic obesity in mice, deer mice, and hamsters. Journal of Parasitology 51: 523-531.
30. Mueller J. F. 1966. The laboratory propagation of Spirometra mansonoides (Mueller, 1935) as an experimental tool. VII. Improved techniques and additional notes on the biology of the cestode. Journal of Parasitology 52: 437-443.
31. Mueller J. F. 1966b. Host-parasite relationships as illustrated by the cestode Spirometra mansonoides. In: Host - Parasite Relationships. Proceedings of the 26th Annual Biology Colloquium, Oregon State University (Edited by McCauley J. E.), pp. 11-58.
32. Mueller J. F. 1968. Growth stimulating effect of experimental sparganosis in thyroidectomised and hypophysectomised rats and comparative activity of different species of Spirometra. Journal of Parasitology 54: 795-801.
33. Mueller J. F. & Reed P. 1968. Growth stimulation induced by infection with Spirometra mansonoides spargana in propylthiouracil-treated rats. Journal of Parasitology 54: 51-54.
34. Mueller J. F. 1970. Quantitative relationship between stimulus and response in growth-promoting effect of Spirometra mansonoides spargana on the hypophysectomized rat. Journal of Parasitology 56: 840-842.
35. Mueller J. F. 1970. Comparison of the growth-promoting effect of Spirometra mansonoides vs three Oriental forms in intact mice and hypophysectomized rats. Journal of Parasitology 56: 842-844.
36. Mueller J. F. 1972. Absence of sparganum growth factor in African Spirometra ssp. Journal of Parasitology 58: 872-875.
37. Odening V. K. & Bockhardt I. 1982. Zwei europäische Spirometra-Formen (Cestodea: Diphyllobothriidae) mit unterschiedlichem sparganum growth factor. Angew Parasitology 23: 15-27.
38. Opuni E. K., Muller R. & Mueller J. F. 1974. Absence of sparganum growth factor in African Spirometra spp. Journal of Parasitology 60: 375-376.
39. Pandian M. R. & Talwar G. P. 1971. Effect of growth hormone on the metabolism of thymus and on the immune response against sheep erythrocytes. Journal of Experimental Medicine 134: 1095-1113.
40. Phares C. K. & Ruegamer W. R. 1972. Pigeon crop sac stimulation due to a factor produced by plerocercoids of the tapeworm, Spirometra mansonoides. Proceedings of the Society for Experimental Biology and Medicine 143: 147-151.
41. Phares C. K. & Ruegamer W. R. 1973. In vitro preparation of a growth factor form plerocercoids of the tapeworm, Spirometra mansonoides. Proceedings of the Society for Experimental Biology and Medicine 142: 374-377.
42. Phares C. K. & Corkum K. C. 1974. Effects of spirometrid plerocercoids on several species of lower vertebrates. Journal of Comparative Biochemistry and Physiology 48A: 525-531.
43. Phares C. K. & Ruegamer W. R. 1976. Effects of growth factor from the tapeworm, Spirometra mansonoides, on a hypophysectomized Rhesus monkey. Proceedings of the 58th Endocrinology Society Meeting, pp. 459.
44. Phares C. K., Hofert J. F. & Pettinger C. L. 1976. Growth stimulation of lymphatic tissue by plerocercoid larvae of the tapeworm. Spirometra mansonoides. General and Comparative Endocrinology 28: 103-106.
45. Phares C. K. & Carroll R. M. 1977. A lipogenic effect in intact male hamsters infected with plerocercoids of the tapeworm. Spirometra mansonoides. Journal of Parasitology 63: 690-693.
46. Phares C. K. & Carroll R. M. 1978. Comparison of the effects of the growth factor produced by Spirometra mansonoides and growth hormone in diabetic-hypophysectomized rats: lipid composition. Journal of Parasitology 64: 401-405.
47. Phares C. K. 1982. The lipogenic effect of the growth factor produced by plerocercoids of the tapeworm, Spirometra mansonoides is not the result of hypothyroidism. Journal of Parasitology 68: 999-1003.
48. Phares C. K. & Ai N. D. 1982. Spirometra mansonoides: effects of plerocercoid infection on glycogen deposition in rats. Journal of Helminthology 56: 315-322.
49. Phares C. K. & Booth B. J. M. 1986. Reduction of lactogenic receptors in female hamster liver due to the hGH analogue produced by plerocercoids of the tapeworm. Spirometra mansonoides. Endocrinology 118: 1102-1109.
50. Phares C. K. & Booth B. J. M. 1986. Suppression of receptors for prolactin and estrogen in rat liver due to treatment with the growth hormone analogue produced by the tapeworm Spirometra mansonoides. Journal of Receptor Research 6: 425-446.
51. Phares C. K. & Booth B. J. M. 1987. Anti-human growth hormone (GH) antibodies cross-react with the GH-like factor form plerocercoids of the tapeworm Spirometra mansonoides. Endocrinology 121: 1839-1844.
52. Phares C. K. & Cox G. S. 1987. Molecular hybridization and immunological data support the hypothesis that the tapeworm, Spirometra mansonoides, has acquired a human growth hormone gene. In: Molecular Paradigms for Eradicating Helminthic Parasites (Edited by MacInnis A. J.), pp. 391-405. Alan R. Liss Company, New York.
53. Phares C. K. 1988. Use of receptor affinity chromatography in purification of the growth hormone-like factor produced by plerocercoids of the tapeworm Spirometra mansonoides. Journal of Receptor Research 8: 645-665.
54. Phares C. K. & Watts D. J. 1988. The growth hormone-like factor produced by the tapeworm Spirometra mansonoides competitively inhibits the binding of human growth hormone to its receptors on IM9 cells. Journal of Parasitology 745: 896-898.
55. Phares C. K., Shaffer J. L. & Heidrick M. L. 1990. Characteristics, distribution and possible evolutionary importance of the human growth hormone-like factor from plerocercoids of the tapeworm genus Spirometra. In: Immune Recognition and Evasion: Molecular Aspects of Host-Parasite Interaction (Edited by Van Der Ploeg L., Cantor C. R. & Vogel H. J.), pp. 149-161. Academic Press, San Diego, California.
56. Phares C. K. & Sharp S. W. 1991. Immuno-enhancement associated with the growth hormone-like factor produced by the tapeworm. Spirometra mansonoides. Experimental and Clinical Endocrinology 10: 179-184.
57. Phares C. K. 1996. The growth hormone-like factor from plerocercoids of the tapeworm Spirometra mansonoides is a multi-functional protein. In: Parasitic Effects on Host Hormones and Behavior (Edited by Beckage N. and Zuk M.), in press. Chapman and Hall, New York.
58. Phares C. K. & Kubik J. 1996. The growth factor from plerocercoids of Spirometra mansonoides is both a growth hormone agonist and a cysteine proteinase. Journal of Parasitology 82: 210-215.
59. Ramaley J. A. & Phares C. K. 1980. Delay of puberty onset due to suppression of growth hormone. Endocrinology 1066: 1989-1993.
60. Ramaley J. A. & Phares C. K. 1900. Delay of puberty onset in mates due to suppression of growth hormone. Neuroendocrinology 36: 321-329.
61. Ruegamer W. R. & Phares C. K. 1974. Effects of age on growth and food efficiency responses in rats infected with tapeworm larvae. Proceedings of the Society for Experimental Biology and Medicine 146: 698-702.
62. Salem M. A. M. & Phares C. K. 1986. Some biochemical effects of the growth hormone analogue produced by plerocercoids larvae of the tapeworm, Spirometra mansonoides on carbohydrate metabolism of adipose tissue from normal, diabetic and hypophysectomize rat. Journal of Parasitology 724: 498-506.
63. Salem M. A. M. & Phares C. K. 1987. Insulin-like effects in the rat of the purified growth factor form Spirometra mansonoides plerocercoids. Proceedings of the Society for Experimental Biology and Medicine 185: 31-38.
64. Salem M. A. M. & Phares C. K. 1989a. The growth factor from plerocercoid larvae of the tapeworm, Spirometra mansonoides stimulates growth but is not diabetogenic. Proceedings of the Society for Experimental Biology and Medicine 191: 187-192.
65. Salem M. A. M. & Phares C. K. 1989b. In vitro insulin-like actions of the growth factor from the tapeworm, Spirometra mansonoides. Proceedings of the Society for Experimental Biology and Medicine 190: 203-210.
66. Sharp S. E., Phares C. K. & Heidrick M. L. 1982. Immunological aspects associated with suppression of hormone levels in rats infected with plerocercoids of Spirometra mansonoides (Cestoda). Journal of Parasitology 686: 993-998.
67. Shiwaku K. & Hirai K. 1982. Growth-promoting effect of Spirometra erinacei (Rudolphi, 1819) plerocercoids in young mice. Japanese Journal of Parasitology 31: 185-195.
68. Shiwaku K., Hirai K., Tsuboi T. & Torii M. 1986. Enhancement of serum somatomedin activity and cartilage mitotic activity in Snell normal and dwarf mice infected with Spirometra erinacei plerocercoids. Japanese Journal of Parasitology 35: 411-417.
69. Song C. Y. & Chappell C. L. 1993. Purification and partial characterization of cysteine proteinase from Spirometra mansoni plerocercoids. Journal of Parasitology 79: 517-524.
70. Steelman S. L., Morgan E. R., Cuccaro A. J. & Glitzer M. S. 1969. Growth hormone-like activity in hypophysectornized rats implanted with Spirometra mansonoides spargana (34453). Proceedings of the Society for Experimental Biology and Medicine 133: 269-273.
71. Steelman S. L., Glitzer M. S., Ostlind D. A. & Mueller J. F. 1971. Biological properties of the growth hormone-like factor from the plerocercoid of Spirometra mansonoides. Recent Progress in Hormone Research 27: 97-120.
72. Torosian M. H. & Donoway R. B. 1991. Growth hormone inhibits tumor metastasis. Cancer 67: 2280-2283.
73. Tseng M. T. & Mueller J. F. 1977. Suppression of somatotrops in rats bearing spargana of Spirometra mansonoides, an ultrastructural study. Journal of Parasitology 63: 168-169.
74. Tsuboi T., Hirai K., Torii M. & Nishida H. 3991. Decrease of liver glycogen content in golden hamsters infected with plerocercoids of Spirometra erinacei. Parasitology Research 77: 320-324.
75. Tsuboi T., Oka K., Hirai K. & Torii M. 1992. Effects of proteinase inhibitors on liver cell growth stimulating activity and cytostolic calcium concentration by the infection of plerocercoids of Spirometra erinacei. Japanese Journal of Parasitology 41suppl: 64.
76. Tsushima T. & Friesen H. G. 1973. Radioreceptor assay for growth hormone. Journal of Clinical Endocrinology and Metabolism 37: 344-348.
77. Tsushima T., Friesen H. G., Chang T. W. & Raben M. S. 1974. Identification of sparganum growth factor by a radioreceptor assay for growth hormone. Biochemical and Biophysical Research Communications 59: 1062-1068.
78. Wang H.-R., Tanihata T., Fukumoto S., Hirai K. & Phares C. K. 1995. Immunohistochemical localization of a 27 kDa protein in the plerocercoids of Spirometra erinacei. Japanese Journal of Parasitology 44: 6-11.
79. Yoon J.-B., Towle H. C. & Seelig S. 1995. Growth hormone induces two mRNA species of the serine protease inhibitor gene family in rat liver. Journal of Biological Chemistry 262: 4284-4289.