Biotechnologia Acta

...

  • Increase font size
  • Default font size
  • Decrease font size
Home Archive 2013 № 6 BIOTECHNOLOGY OF THE FISH AQUACULTURE L. P. Buchatsky
Print PDF

ISSN 2410-7751 (Print)
ISSN 2410-776X (Online)

Biotechnologia Acta
v. 6, No. 6, 2013


"Biotechnologia Acta" v. 6, no 6, 2013
doi: 10.15407/biotech6.06.045
Р. 45-57, Bibliography 90, Russian.
Universal Decimal classification: 621.59: 597 114.78

BIOTECHNOLOGY OF THE FISH AQUACULTURE

L. P. Buchatsky

Institute for Fisheries of Ukrainian Academy of Agrarian Sciences, Kyiv, Ukraine

The latest progress in biotechnology on fish aquaculture and different modern methods of investigations for increasing of fish productivity in aquaculture are analyzed. Except for the applied aspect, the use of modern biotechnological methods of investigations opens new possibilities for fundamental researches of sex-determining mechanisms, polyploidy, distant hybridization, and developmental biology of bony fishes. Review contains examples of utilizing modern biotechnology methods to obtain transgenic fishes with accelerated growth and for designing surrogate fishes. Methods for receiving unisexual shoals of salmon and sturgeon female fishes with the view of obtaining a large quantity of caviar, as well as receiving sterile (triploid) fishes are analyzed. Great attention is given to androgenesis, particularly to disperm one, in connection with the problem of conserving rare and vanishing fish species using only sperm genetic material. Examples how distant hybrids may be obtained with the use of disperm androgenesis and alkylated DNA are given. Methods of obtaining fish primordium germ cells, recent developments in cultivation of fish stem cells and their use in biotechnology, as well as ones of transplantation of oogonium and spermatogonium to obtain surrogate fishes. The examples of successful experiments on spermatogonial xenotransplantation and characteristic of antifreezing fish proteins and also the prospect of their practical usage are given.

Key words: fishes, grows acceleration, reproduction, sterilization, androgenesis, stem cells, transplantation, antifreeze proteins.

© Palladin Institute of Biochemistry of National Academy of Sciences of Ukraine, 2008

  • References
    • 1. Vasil I. K. Biotechnology and food security for the 21st century: a real-world perspective. Nat. Biotechnol. 1998, V. 16, P. 399–400.
      http://dx.doi.org/10.1038/nbt0598-399
      PMid:9592375

      2. Hew C. L., Fletcher G. L. The role of aquatic biotechnology in aquaculture. Aquaculture. 2001, V. 197, P. 191-204.
      http://dx.doi.org/10.1016/S0044-8486(01)00587-7

      3. Aparicio S., Chapman J., Stupka E. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science. 2002, 297 (5585), 1301-1310.
      http://dx.doi.org/10.1126/science.1072104
      PMid:12142439

      4. DaSilva E. J. The colours of  Biotechnology: Science, Development and Humankinde. Electr. J. Biotechnol. Edit. art. 2004, 7 (3), 1.

      5. Palmiter R. D., Brinste R. L., Hammer R. E. Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes. Nature. 1982, V. 300, P. 611–615.
      http://dx.doi.org/10.1038/300611a0
      PMid:6958982

      6. Du S. J., Gong Z., Fletcher G. L. Growth enhancement in transgenic Atlantic salmon by the use of an all fish chimeric growth hormone gene construct. Biol. Technol. 1992, 10 (2), 176–181.
      http://dx.doi.org/10.1038/nbt0292-176

      7. Rasmussen R. S., Morrissey M. T. Biotechnology in aquaculture: transgenic and polyploidy. Comprehensive reviews in food science and food safety. 2007, V. 6, P. 2-16.
      http://dx.doi.org/10.1111/j.1541-4337.2007.00013.x

      8. Wan H., He J., In B. Generation of two-color transgenic zebrafish using the green and red flguorescent protein receptor genes, gfp and rfp. Mar. Biotechnol. 2002, 4 (2), 146-154.
      http://dx.doi.org/10.1007/s10126-001-0085-3
      PMid:14961274

      9. Takeuchi Y., Yoshizaki G., Kobayashi T. Mass isolation of primordial germ cells from transgenic rainbow trout carrying the green fluorescent protein gene driven by the vasa gene promoter. Biol. Reprod. 2002, V. 67, P. 1087-1092.
      http://dx.doi.org/10.1095/biolreprod67.4.1087
      PMid:12297522

      10. Yoshizaki G., Tago Y., Takeuchi Y. Green fluorescent protein labeling of primordial germ cells using a nontransgenic method and its application for germ cell transplantation in salmonidae. Biol. Reprod. 2005, V. 73, P. 88-93.
      http://dx.doi.org/10.1095/biolreprod.104.034249
      PMid:15744027

      11. Yamaha E., Saito T., Goto-Cazeto R. Developmental biotechnology for aquaculture, with special reference to surrogate production in teleost fishes. J. Sea Res. 2007, V. 58, P. 8-22.
      http://dx.doi.org/10.1016/j.seares.2007.02.003

      12. Shikina S., Ihara S., Yoshizaki G. Culture conditions for maintaining the survival and mitotic activity of rainbow trout transplantable type A spermatogonia. Mol. Reprod. Dev. 2008, V. 75, P. 529-537.
      http://dx.doi.org/10.1002/mrd.20771
      PMid:18022822

      13. Alvarez M. C., Bejar J., Chen S. Fish ES cell and applications to biotechnology. Marine Biotechnol. 2007, V. 9, P. 117-127.
      http://dx.doi.org/10.1007/s10126-006-6034-4
      PMid:17089084

      14. Buchatskyi L. P. Fish Transgenesis. Rybn. gospHomelskyi. 2000, V. 56-57, P. 51-61.

      15. Devlin R. H., Nagahama Y. Sex determination in fish: an overview of genetic, physiological, and environmental influences. Aquaculture. 2002, V. 208, P. 191-364.
      http://dx.doi.org/10.1016/S0044-8486(02)00057-1

      16. Devlin R. H., Park L., Sakhrani D. M. Variation of Y-chromosome markers in chinoock salmon (Oncorhynchus tshawytscha) populations. Can. J. Fish. Aquat. Sci. 2005, V. 62, P. 1386-1399.
      http://dx.doi.org/10.1139/f05-048

      17. Brunelli J. P., Wertzler K. J., Sundin K. Y-specific sequences and polymorphisms in rainbow trout and chinoock salmon. Genome. 2008, V. 51, P. 739-748.
      http://dx.doi.org/10.1139/G08-060

      18. Lanes C. F., Sampaio L. A., Marins L. F. Evaluation of DNAse activity in seminal plasma and uptake of exogenous DNA by spermatozoa of the brazilian flounder Paralichthys orbignyanus. Theriogenology. 2009, V. 71, P. 525-533.
      http://dx.doi.org/10.1016/j.theriogenology.2008.08.019

      19. Maclean N., Laight, R. J. Transgenic fish: an evaluation of benefits and risks. Fish. 2000, N 1, P. 146–172.

      20. Homelskyi B. I., Hrunina A. S. Artificial polyploidy fish and possibility of its use in fish farming. TSNIIITEIRKh Overview. 1988, V. 1, P. 1-25. (In Russian).

      21. Horbunov L. V., Buchatskyi L. P. Cryopreservation of gametes and embryos of animals. VPTs Kyiv. un-tet. 2005, 325 p. (In Russian).

      22. Grunina A. S., Recoubratsky A. V., Neyfakh A. A. Induced diploid androgenesis in sturgeons. Sturgeon Quart. 1995, 3 (3), 6–7.

      23. Araki K., Shinma H., Nagoya H. Androgenetic diploids of rainbow trout (Oncorhynchus mykiss) produced by fused sperm. Can. J. Fish. Aquat. Sci. 1995, V. 52, P. 892–896.
      http://dx.doi.org/10.1139/f95-089

      24. Hrunina A. S., Rekurbatskiy A.V. Androgenesis fish, or only the seed from the male. Priroda. 2006, N 11, P. 25–31. (In Russian).

      25. Hrunina A. S., Rekurbatskiy A.V., Tsvetkova L. I. Dispermic androgenesis sturgeons using cryopreserved sperm: obtaining androgenetic offspring of the Siberian sturgeon and androgenetic hybrids between Siberian and Russian sturgeon. Ontogenez. 2011, 42 (2), 133–145. (In Russian).

      26. Kirankumar S., Pandian T. J. Use of heterologous sperm for the dispermic induction of androgenesis in barbs. J. Fish Biol. 2004, V. 64, P. 1485–1497.
      http://dx.doi.org/10.1111/j.0022-1112.2004.00398.x

      27. Clifton J. D, Pandin T. J. Dispermic induction of intercpecific androgenesis in the fish, Buenos Aires tetra using surrogate eggs widow tetra. Curr. Sci. 2008, 95 (1), 64.

      28. Buchatskii L.P., Potopalskyi A.I., Zaika L.A. The use of alkylated DNA hybrids remote to display fish. Tvarinnitstvo Ukr. 2010, N 4, P. 21–23. (In Ukrainian).

      29. Buchatskii L.P., Potopalskii A. I, Zaika L.A. The patent for utility model N 44303 “Method for hybrids fish obtaining”. Registered 25.09.2009.  (In Ukrainian).

      30. Melamed P., Gong Z., Fletcher G. The potential impact of modern biotechnology on fish aquaculture. Aquaculture. 2002, V. 204, P. 255–269.
      http://dx.doi.org/10.1016/S0044-8486(01)00838-9

      31. Yoshizaki G., Ichikawa M., Hayashi M. Sexual plasticity of ovarian germ cells in rainbow trout. Development. 2010, V. 137, P. 1227–1230.
      http://dx.doi.org/10.1242/dev.044982

      32. Metalnikova K. V. Progeny reversantov steelhead. Ribn. khoz. 1991, N 12, P. 59–61. (In Russian).

      33. Pavlov E. D., Nhuen Vet Tui, Nhuen Ti Tu. Status of sexual glands of young triploid trout Oncorhynchus mykiss in conditions of Southern Vietnam during artificial inversion of sex. Vopr. ikhtiol. 2010, 50 (5), 675–684. (In Russian).

      34. Raz E., Reichman-Fried M. Attraction rules: germ cell migration in zebrafish. Curr. Opin. Genet. Develop. 2006, V. 16, P. 355–359.
      http://dx.doi.org/10.1016/j.gde.2006.06.007

      35. Yoshizaki G., Sakatani S., Tominaga H. Cloning and characterization of a vasa-like gene in rainbow trout and its expression in the germ cell lineage. Mol. Reprod. Develop. 2000, V. 55, P. 364–371.
      http://dx.doi.org/10.1002/(SICI)1098-2795(200004)55:4<364::AID-MRD2>3.0.CO;2-8

      36. Takashima F., Patino R., Nomura M. Histological studies on the sex differentiation in rainbow trout. Bull. Japan. Soc. Sci. Fish. 1982, V. 46, P. 1317–1322.
      http://dx.doi.org/10.2331/suisan.46.1317

      37. Raz E. The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 2000, N 1, P. 1017.

      38. Yoshizaki G., Takeuchi Y., Sakatani S. Germ cell–specific expression of green fluorescent protein in transgenic rainbow trout under control of the rainbow trout vasa–like gene promoter. Int. J. Dev. Biol. 2000, V. 44, P. 323–326.

      39. Yoshizaki G., Fujinuma K., Iwasaki Y. Spermatogonial transplantation in fish: a novel method for the preservation of genetic resources. Comp. Biochem. Physiol. Part D. Genom. Proteom. 2011, 6 (1), 55–61.
      http://dx.doi.org/10.1016/j.cbd.2010.05.003

      40. Knaut H., Steinbeisser H., Schwarz H. An evolutionary conserved region in the vasa 3′UTR targets RNA translation to the germ cells in the zebrafish. Curr. Biol. 2002, N 12, P. 454–466.
      http://dx.doi.org/10.1016/S0960-9822(02)00723-6

      41. Wolkе U., Weidinger G., Köprunner M. Multiple levels of posttranscriptional control lead to germ line-specific gene expression in the zebrafish. Curr. Biol. 2002, V. 12, P. 289–294.

      42. Okutsu T., Suzuki K., Takeuchi Y. Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. Proc. Natl. Acad. Sci. USA. 2006, V. 103, P. 2725–2729.
      http://dx.doi.org/10.1073/pnas.0509218103

      43. Yano A., Suzuki K., Yoshizaki G. Flowcytometric isolation of testicular germ cells from rainbow trout (Oncorhynchus mykiss) carrying the greenfluorescent protein gene driven by trout vasa regulatory regions. Biol. Reprod. 2008, V. 78, P. 151–158.
      http://dx.doi.org/10.1095/biolreprod.107.064667

      44. Schulz R. W, de França L. R., Lareyre J. J. Spermatogenesis in fish. Gen. Comp. Endocrinol. 2010, V. 165, P. 390–411.
      http://dx.doi.org/10.1016/j.ygcen.2009.02.013

      45. Yoshizaki G., Ichikawa M., Hayashi M. Sexual plasticity of ovarian germ cells in rainbow trout. Development. 2010, V. 137, P.1227–1230.
      http://dx.doi.org/10.1242/dev.044982

      46. Loir M. Spermatogonia of rainbow trout: I. Morphological characterization, mitotic activity, and survival in primary cultures of testicular cells. Mol. Reprod. Dev. 1999, V. 53, P. 422–433.
      http://dx.doi.org/10.1002/(SICI)1098-2795(199908)53:4<422::AID-MRD8>3.0.CO;2-V

      47. Okutsu T., Yano A., Nagasawa K. Manipulation of fish germ cell: visualization, cryopreservation and transplantation. J. Reprod. Develop. 2006, V. 52, P. 685–693.
      http://dx.doi.org/10.1262/jrd.18096

      48. Okutsu T., Shikina S., Kanno M. Production of trout offspring from triploid salmon parents. Science. 2007, V. 317, P. 1517.
      http://dx.doi.org/10.1126/science.1145626

      49. Okutsu T., Takeuchi Y., Yoshizaki G. Spermatogonial transplantation in fish: production of trout offspring from salmon parents. Tsukamoto K. (Ed). Fisheries for global welfare and environment. 5th World Fisheries Congress. 2008, P. 209–219.

      50. Lacerda S. M., Batlouni S. R., Silva S. B. Germ cell transplantation in fish: the Nile–tilapia model. Anim. Reprod. 2006, N 3, P. 146–159.

      51. Lacerda S. M., Batlouni S. R., Assis L. Germ cell transplantation in tilapias (Oreochromis niloticus). Cybium. 2008, V. 32, P. 115–118.

      52. Lacerda S. M., Batlouni S. R., Costa G. M. A new and fast technique to generate offspring after germ cells transplantation in adult fish: the nile tilapia (Oreochromis niloticus) model. PLoS One. 2010, N 5, e 10740.

      53. Majhi S. K., Hattori R. S., Yokota M. Germ cell transplantation using sexually competent fish: an approach for rapid propagation of endangered and valuable germlines. PLoS One. 2009, N 4, e 6132.

      54. Nagasawa K., Shikina S., Takeuchi Y. Lymphocyte antigen 75 (Ly75/CD205) is a surface marker on mitotic germ cells in rainbow trout. Biol. Reprod. 2010, 83 (4), 597–606.
      http://dx.doi.org/10.1095/biolreprod.109.082081

      55. Hong Y., Liu T., Zhao H. Establishment of a normal medaka fish spermatogonial cell line capable of sperm production in vitro. Proc. Natl. Acad. Sci. USA. 2004, V. 101, P. 8011–8016.
      http://dx.doi.org/10.1073/pnas.0308668101

      56. Carrasco L. A., Doroshov S., Penman D. J. Long-term, quantitative analysis of gametogenesis in autotriploid rainbow trout, Oncorhynchus mykiss. J. Reprod. Fertil. 1998, V. 113, P. 197–210.
      http://dx.doi.org/10.1530/jrf.0.1130197

      57. Lin S., Long W., Chen J. Production of germ-line chimeras in zebrafish by cell transplants from genetically pigmented to albino embryos. Proc. Natl. Acad. Sci. USA. 1992, V. 89, P. 4519–4523.
      http://dx.doi.org/10.1073/pnas.89.10.4519

      58. Nakamura S., Kobayashi K., Nishimura T. Identification of germline stem cells in the ovary of the teleost medaka. Science. 2010, V. 328, P. 1561–1563.
      http://dx.doi.org/10.1126/science.1185473

      59. Nobrega R. H., Batlouni S. R., Franca L. R. An overview of functional and stereological evaluation of spermatogenesis and germ cell transplantation in fish. Fish Physiol. Biochem. 2009, V. 35, P. 197–206.
      http://dx.doi.org/10.1007/s10695-008-9252-z

      60. Collares T., Campos V. F., Seixas F. K. Transgene transmission in south american catfish (Rhamdia quelen) larvae by sperm–mediated gene transfer. J. Biosci. 2010, V. 35, P. 39–47.
      http://dx.doi.org/10.1007/s12038-010-0006-6

      61. Collodi P., Kamei Y., Ernst T. Culture of cells from zebrafish (Brachydanio rerio) embryo and adult tissues. Cell. Biol. Toxicol. 1992, N 8, P. 43–61.
      http://dx.doi.org/10.1007/BF00119294

      62. Yi M., Hong N., Hong Y. Generation of medaka fish haploid embryonic stem cells. Science. 2009, V. 326, P. 430–433.
      http://dx.doi.org/10.1126/science.1175151

      63. Sun L., Bradford C. S., Ghosh C. Es-like cell cultures derived from early zebrafish embryos. Mol. Mar. Biol. Biotechnol. 1995, N 4, P. 193–199.

      64. Fan L., Crodian J., Collodi P. Culture of embryonic stem cell lines from zebrafish. Meth. Cell Biol. 2004, V. 76, P. 151–160.
      http://dx.doi.org/10.1016/S0091-679X(04)76009-4

      65. Ma C., Fan L., Ganassin R. Production of zebrafish germ–line chimeras from embryo cell cultures. Proc. Natl. Acad. Sci. USA. 2001, V. 98, P. 2461–2466.
      http://dx.doi.org/10.1073/pnas.041449398

      66. Alvares M. C., Bejar J., Chen S. Fish ES cells and applications to biotechnology. Marine Biotechnol. 2006, V. 9, P. 117–127.
      http://dx.doi.org/10.1007/s10126-006-6034-4

      67. Li Z., Bhat N., Manali D. Medaka cleavage embryos are capable of generating ES–like cell cultures. Int. J. Biol. Sci. 2011, N 7, P. 418–425.
      http://dx.doi.org/10.7150/ijbs.7.418

      68. Yi M., Hong N., Hong Y. Generation of medaka fish haploid embryonic stem cells. Science. 2009, V. 326, P. 430–433.
      http://dx.doi.org/10.1126/science.1175151

      69. Hong N., Li Z., Hong Y. Fish stem cell cultures. Int. J. Biol. Sci. 2011, 7 (4), 392–402.
      http://dx.doi.org/10.7150/ijbs.7.392

      70. Shikina S., Yoshizaki G. Improved in vitro culture conditions to enhance the survival, mitotic activity, and transplantability of rainbow trout type A spermatogonia. Biol. Reprod. 2010, V. 83, P. 268–276.
      http://dx.doi.org/10.1095/biolreprod.109.082123

      71. Bejar J., Hong Y., Alvarez M. C. An ES–like cell line from the marine fish sparus aurata: characterization and chimaera production. Transgenic Res. 2002, V. 11, P. 279–289.
      http://dx.doi.org/10.1023/A:1015678416921

      72. Chen S. L., Ye H., Sha Q. Derivation of a pluripotent embryonic cell line from red sea bream blastulas. J. Fish. Biol. 2003, V. 63, P. 10.
      http://dx.doi.org/10.1046/j.1095-8649.2003.00192.x

      73. Chen S. L., Sha Z. X., Ye H. Q. Pluripotency and chimera competence of an embryonic stem cell line from the sea perch (Lateolabrax japonicus). Mar. Biotechnol. 2007, V. 9, P. 82–91.
      http://dx.doi.org/10.1007/s10126-006-6050-1

      74. Parameswaran V., Shukla R., Bhonde R. Development of a pluripotent ES–like cell line from Asian sea bass (Lates calcarifer) – an oviparous stem cell line mimicking viviparous es cells. Mar. Biotechnol. 2007, V. 9, P. 766–775.
      http://dx.doi.org/10.1007/s10126-007-9028-y

      75. Holen E., Hamre K. Towards obtaining long term embryonic stem cell like cultures from a marine flatfish, Scophthalmus maximus. Fish. Physiol. Biochem. 2004, V. 29, P. 245–252.
      http://dx.doi.org/10.1023/B:FISH.0000045725.01192.44

      76. Holen E., Kausland A., Skjaerven K. Embryonic stem cells isolated from atlantic cod (Gadus morhua) and the developmental expression of a stage–specific transcription factor ac-pou2. Mar. Biotechnol. 2010, 36 (4), 1029–39.
      http://dx.doi.org/10.1007/s10695-010-9381-z

      77. Campbell K. H., McWhir J., Ritchie W. A. Sheep cloned by nuclear transfer from a cultured cell line. Nature. 1996, V. 380, P. 64–66.
      http://dx.doi.org/10.1038/380064a0

      78. Chen H., Yi Y., Chen M. Studies on the developmental potentiality of cultured cell nuclei of fish. Int. J. Biol. Sci. 2010, V. 6, P. 192–198.
      http://dx.doi.org/10.7150/ijbs.6.192

      79. Hong N., Li Z., Hong Y. Fish stem cultures. Int. J. Biol. Sci. 2011, 7 (40), 392–402.
      http://dx.doi.org/10.7150/ijbs.7.392

      80. Patolsky F., Zheng G. F., Hayden O. Electrical detection of single viruses. Proc. Natl. Acad. Sci. USA. 2004, V. 101, P. 14017–14022.
      http://dx.doi.org/10.1073/pnas.0406159101

      81. Li Q. L., Mahendra, S., Lyon D. Y. Antimicrobial nanomaterials for water disinfection and microbial control: potential applications and implications. Water Res. 2008, V. 42, P. 4591–4602.
      http://dx.doi.org/10.1016/j.watres.2008.08.015

      82. Pradeep T., Anshup C. Noble metal nanoparticles for water purification: a critical review. Thin Solid Films. 2009, V. 517, P. 6441–6478.
      http://dx.doi.org/10.1016/j.tsf.2009.03.195

      83. Rud Yu. P., Prilutska S. V., Buchatskii L.P. Application of C60-fullerenes for photodynamic inactivation of  mosquitoes irydoviruses. Patent invention. 2012, Bul. N 2, 05.01.2012.

      84. Rud Yu., Buchatsky L., Prilutskyy Yu. Using C60 fullerenes for photodynamic inactivation of mosquito iridescent virus. J. Enz. Inhib. Med. Chem. 2012, 27 (4), 614–617.
      http://dx.doi.org/10.3109/14756366.2011.601303

      85. Buchatskiy L.P., Starodub N. F., Nogarev A. V. The use of surface plasmon resonance for the rapid diagnosis of retroviral infections fish. Tez. Vseros. konf. «Probl. patol. immunol. okhr. zdor. ryb i dr. hidrobiont.». Borok. 2003, P. 17–18. (In Russian).

      86. Buchatsky L. P., Starodub N. F. Immune sensor based on surface plasmon resonance for express control of fish retroviral infection. Proc. of the 2-nd bilateral conf. «Aquatic and marine animal health». Shepherdstown. 2003, P. 15.

      87. Rubinsky B., Arav A., Fletcher G. L. Hypothermic protection: a fundamental property of antifreeze proteins. Biochem. Biophys. Res. Commun. 1991, V. 180, 566–571.
      http://dx.doi.org/10.1016/S0006-291X(05)81102-7

      88. Tablin F., Oliver A. E., Walker N. J. Membrane phase transition of intact human platelets: correlation with cold-induced activation. J. Cell Physiol. 1996, V. 168, P. 305–313.
      http://dx.doi.org/10.1002/(SICI)1097-4652(199608)168:2<305::AID-JCP9>3.0.CO;2-T

      89. Low W. K., Miao M., Ewart K. V. Skin-type antifreeze protein from the shorthorn sculpin, Myoxocephalus scorpius: expression and characterization of 9,700 recombinant protein. J. Biol. Chem. 1998, V. 273, P. 23098–23103.
      http://dx.doi.org/10.1074/jbc.273.36.23098

      90. Hays L. M., Feeney R. E., Crowe L. M. Antifreeze glycoproteins inhibit leakage from liposomes during thermotropic  phase transitions. Proc. Natl. Acad. Sci. USA. 1996, V. 93, P. 6835–6840.
      http://dx.doi.org/10.1073/pnas.93.13.6835