Skip to main content

3D Sponge-Matrix Histoculture: An Overview

  • Protocol
  • First Online:

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1760))

Abstract

Three-dimensional cell culture and tissue culture (histoculture) is much more in vivo-like than 2D culture on plastic. Three-dimensional culture allows investigation of crucial events in tumor biology such as drug response, proliferation and cell cycle progression, cancer cell migration, invasion, metastasis, immune response, and antigen expression that mimic in vivo conditions. Three-dimensional sponge-matrix histoculture maintains the in vivo phenotype, including the formation of differentiated structures of normal and malignant tissues, perhaps due to cells maintaining their natural shape in a sponge-gel matrix such as Gelfoam®. Sponge-matrix histoculture can also support normal tissues and their function including antibody-producing lymphoid tissue that allows efficient HIV infection, hair-growing skin, excised hair follicles that grow hair, pluripotent stem cells that form nerves, and much more.

This is a preview of subscription content, log in via an institution.

Buying options

eBook
USD   39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   54.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Springer Nature is developing a new tool to find and evaluate Protocols. Learn more

References

  1. Folkman J, Moscona A (1978) Role of cell shape in growth control. Nature 273:345–349

    Article  CAS  PubMed  Google Scholar 

  2. Hoffman RM (1993) To do tissue culture in two or three dimensions? That is the question. Stem Cells 11:105–111

    Article  CAS  PubMed  Google Scholar 

  3. Miller BE, Miller FR, Heppner GH (1984) Assessing tumour drug sensitivity by a new in vitro assay which preserves tumour heterogeneity and subpopulation interactions. J Cell Physiol 3(Suppl):105–116

    Article  CAS  Google Scholar 

  4. Miller BE, Miller FR, Heppner GH (1985) Factors affecting growth and drug sensitivity of mouse mammary tumor lines in collagen gel cultures. Cancer Res 45:4200–4205

    CAS  PubMed  Google Scholar 

  5. Yano S, Zhang Y, Miwa S, Tome Y, Hiroshima Y, Uehara F, Yamamoto M, Suetsugu A, Kishimoto H, Tazawa H, Zhao M, Bouvet M, Fujiwara T, Hoffman RM (2014) Spatial-temporal FUCCI imaging of each cell in a tumor demonstrates locational dependence of cell cycle dynamics and chemoresponsiveness. Cell Cycle 13:2110–2119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Teicher BA, Herman TS, Holden S, Wang YY, Pfeffer MR, Crawford JW, Frei E III (1990) Tumor resistance to alkylating agents conferred by mechanisms operative only in vivo. Science 247:1457–1461

    Article  CAS  PubMed  Google Scholar 

  7. Kobayashi HI, Man S, Graham C, Kapitain SJ, Teicher BA, Kerbel RS (1993) Acquired multicellular mediated resistance to alkylating agents in cancer. Proc Natl Acad Sci U S A 90:3294–3298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Yano S, Miwa S, Kishimoto H, Uehara F, Tazawa H, Toneri M, Hiroshima Y, Yamamoto M, Urata Y, Kagawa S, Bouvet M, Funiwara T, Hoffman RM (2015) Targeting tumors with a killer-reporter adenovirus for curative fluorescence-guided surgery of soft-tissue sarcoma. Oncotarget 6:13133–13148

    Article  PubMed  PubMed Central  Google Scholar 

  9. Yano S, Miwa S, Kishimoto H, Toneri M, Hiroshima Y, Yamamoto M, Bouvet M, Urata Y, Tazawa H, Kagawa S, Funiwara T, Hoffman RM (2015) Experimental curative fluorescence-guided surgery of highly invasive glioblastoma multiforme selectively labeled with a killer-reporter adenovirus. Mol Ther 23:1182–1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Yano S, Hiroshima Y, Maawy A, Kishimoto H, Suetsugu A, Miwa S, Toneri M, Yamamoto M, Katz MHG, Fleming JB, Urata Y, Tazawa H, Kagawa S, Bouvet M, Fujiwara T, Hoffman RM (2015) Color-coding cancer and stromal cells with genetic reporters in a patient-derived orthotopic xenograft (PDOX) model of pancreatic cancer enhances fluorescence-guided surgery. Cancer Gene Ther 22:344–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Yano S, Zhang Y, Miwa S, Kishimoto H, Urata Y, Bouvet M, Kagawa S, Fujiwara T, Hoffman RM (2015) Precise navigation surgery of tumours in the lung in mouse models enabled by in situ fluorescence labelling with a killer-reporter adenovirus. BMJ Open Respir Res 2:e000096

    Article  PubMed  PubMed Central  Google Scholar 

  12. Yano S, Takehara K, Miwa S, Kishimoto H, Hiroshima Y, Murakami T, Urata Y, Kagawa S, Bouvet M, Fujiwara T, Hoffman RM (2016) Improved resection and outcome of colon-cancer liver metastasis with fluorescence-guided surgery using in situ GFP labeling with a telomerase-dependent adenovirus in an orthotopic mouse model. PLoS One 11:e0148760

    Article  PubMed  PubMed Central  Google Scholar 

  13. Yano S, Miwa S, Kishimoto H, Urata Y, Tazawa H, Kagawa S, Bouvet M, Fujiwara T, Hoffman RM (2016) Eradication of osteosarcoma by fluorescence-guided surgery with tumor labeling by a killer-reporter adenovirus. J Orthopaedic Res 34:836–844

    Article  CAS  Google Scholar 

  14. Yano S, Takehara K, Miwa S, Kishimoto H, Tazawa H, Urata Y, Kagawa S, Bouvet M, Fujiwara T, Hoffman RM (2016) Fluorescence-guided surgery of a highly-metastatic variant of human triple-negative breast cancer targeted with a cancer-specific GFP adenovirus prevents recurrence. Oncotarget 7:75635–75647

    PubMed  PubMed Central  Google Scholar 

  15. Leighton J (1960) The propagation of aggregates of cancer cells: implications for therapy and a simple method of study. Cancer Chemother Rep 9:71–72

    CAS  PubMed  Google Scholar 

  16. Leighton J, Kalla R, Turner JM Jr, Fennell RH Jr (1960) Pathogenesis of tumor invasion. II. Aggregate replication. Cancer Res 20:575–586

    CAS  PubMed  Google Scholar 

  17. Leighton J (1959) Aggregate replication, a factor in the growth of cancer. Science 129(3347):466–467

    Article  CAS  PubMed  Google Scholar 

  18. Leighton J, Kalla R, Kline I, Belkin M (1959) Pathogenesis of tumor invasion. I. Interaction between normal tissues and transformed cells in tissue culture. Cancer Res 19:23–27

    CAS  PubMed  Google Scholar 

  19. Dawe CJ, Potter M, Leighton J (1958) Progressions of a reticulum-cell sarcoma of the mouse in vivo and in vitro. J Natl Cancer Inst 21:753–781

    CAS  PubMed  Google Scholar 

  20. Leighton J (1957) Contributions of tissue culture studies to an understanding of the biology of cancer: a review. Cancer Res 17:929–941

    CAS  PubMed  Google Scholar 

  21. Kline I, Leighton J, Belkin M, Orr HC (1957) Some observations on the response of four established human cell strains to hydrocortisone in tissue culture. Cancer Res 17:780–784

    CAS  PubMed  Google Scholar 

  22. Leighton J, Kline I, Belkin M, Legallais F, Orr HC (1957) The similarity in histologic appearance of some human cancer and normal cell strains in sponge-matrix tissue culture. Cancer Res 17:359–363

    CAS  PubMed  Google Scholar 

  23. Leighton J, Kline I, Belkin M, Orr HC (1957) Effects of a podophyllotoxin derivative on tissue culture systems in which human cancer invades normal tissue. Cancer Res 17:336–344

    CAS  PubMed  Google Scholar 

  24. Leighton J, Kline I, Belkin M, Tetenbaum Z (1956) Studies on human cancer using sponge-matrix tissue culture. III. The invasive properties of a carcinoma (strain HeLa) as influenced by temperature variations, by conditioned media, and in contact with rapidly growing chick embryonic tissue. J Natl Cancer Inst 16:1353–1373

    CAS  PubMed  Google Scholar 

  25. Leighton J, Kline I, Orr HC (1956) Transformation of normal human fibroblasts into histologically malignant tissue in vitro. Science 123:502

    Article  CAS  PubMed  Google Scholar 

  26. Leighton J (1954) The growth patterns of some transplantable animal tumors in sponge matrix tissue culture. J Natl Cancer Inst 15:275–293

    CAS  PubMed  Google Scholar 

  27. Leighton J, Kline I (1954) Studies on human cancer using sponge matrix tissue culture. II. Invasion of connective tissue by carcinoma (strain HeLa). Tex Rep Biol Med 12:865–873

    CAS  PubMed  Google Scholar 

  28. Leighton J (1954) Studies on human cancer using sponge matrix tissue culture. I. The growth patterns of a malignant melanoma, adenocarcinoma of the parotid gland, papillary adenocarcinoma of the thyroid gland, adenocarcinoma of the pancreas, and epidermoid carcinoma of the uterine cervix (Gey's HeLa strain). Tex Rep Biol Med 12:847–864

    CAS  PubMed  Google Scholar 

  29. Leighton J (1951) A sponge matrix method for tissue culture; formation of organized aggregates of cells in vitro. J Natl Cancer Inst 12:545–561

    CAS  PubMed  Google Scholar 

  30. St Croix B, Florenes VA, Rak JW, Flanagan M, Bhattacharya N, Slingerland JM, Kerbel RS (1996) Impact of the cyclin-dependent kinase inhibitor p27Kip1 on resistance of tumor cells to anticancer agents. Nat Med 2:1204–1210

    Article  CAS  PubMed  Google Scholar 

  31. Chabner BA (ed) (1983) Rational basis for chemotherapy. Liss, New York

    Google Scholar 

  32. Vescio RA, Redfern CH, Nelson TJ, Ugoretz S, Stern PH, Hoffman RM (1987) In vivo-like drug responses of human tumors growing in three-dimensional gel-supported, primary culture. Proc Natl Acad Sci U S A 84:5029–5033

    Google Scholar 

  33. Geller J, Sionit LR, Connors KM, Hoffman RM (1992) Measurement of androgen sensitivity in the human prostate in in vitro three-dimensional histoculture. Prostate 21:269–278

    Article  CAS  PubMed  Google Scholar 

  34. Li L, Margolis LB, Hoffman RM (1991) Skin toxicity determined in vitro by three-dimensional, native-state histoculture. Proc Natl Acad Sci U S A 88:1908–1912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hoffman RM (2010) Histocultures and their use. In: Encyclopedia of life sciences. Wiley, Hoboken. (Published Online)

    Google Scholar 

  36. Li L, Margolis LB, Paus R, Hoffman RM (1992) Hair shaft elongation, follicle growth, and spontaneous regression in long-term, gelatin sponge-supported histoculture of human scalp skin. Proc Natl Acad Sci U S A 89:8764–8768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Cao W, Li L, Mii S, Amoh Y, Liu F, Hoffman RM (2015) Extensive hair shaft elongation by isolated mouse whisker follicles in very long-term Gelfoam® histoculture. PLoS One 10:e0138005

    Article  PubMed  PubMed Central  Google Scholar 

  38. Mii S, Duong J, Tome Y, Uchugonova A, Liu F, Amoh Y, Saito N, Katsuoka K, Hoffman RM (2013) The role of hair follicle nestin-expressing stem cells during whisker sensory-nerve growth in long-term 3D culture. J Cell Biochem 114:1674–1684

    Article  CAS  PubMed  Google Scholar 

  39. Glushakova S, Baibakov B, Margolis LB, Zimmerberg J (1995) Infection of human tonsil histocultures: a model for HIV pathogenesis. Nature Med 1:1320–1322

    Article  CAS  PubMed  Google Scholar 

  40. Chishima T, Yang M, Miyagi Y, Li L, Tan Y, Baranov E, Shimada H, Moossa AR, Penman S, Hoffman RM (1997) Governing step of metastasis visualized in vitro. Proc Natl Acad Sci U S A 94:11573–11576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Chishima T, Miyagi Y, Li L, Tan Y, Baranov E, Yang M, Shimada H, Moossa AR, Hoffman RM (1997) Use of histoculture and green fluorescent protein to visualize tumor cell host interaction. In Vitro Cell Dev Biol 33:745–747

    Article  CAS  Google Scholar 

  42. Yano S, Miwa S, Mii S, Hiroshima Y, Uehara F, Kishimoto H, Tazawa H, Zhao M, Bouvet M, Fujiwara T, Hoffman RM (2015) Cancer cells mimic in vivo spatial-temporal cell-cycle phase distribution and chemosensitivity in 3-dimensional Gelfoam® histoculture but not 2-dimensional culture as visualized with real-time FUCCI imaging. Cell Cycle 14:808–819

    Google Scholar 

  43. Yano S, Miwa S, Mii S, Hiroshima Y, Uehara F, Yamamoto M, Kishimoto H, Tazawa H, Bouvet M, Fujiwara T, Hoffman RM (2014) Invading cancer cells are predominantly in G0/G1 resulting in chemoresistance demonstrated by real-time FUCCI imaging. Cell Cycle 13:953–960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Tome Y, Uehara F, Mii S, Yano S, Zhang L, Sugimoto N, Maehara H, Bouvet M, Tsuchiya H, Kanaya F, Hoffman RM (2014) 3-dimensional tissue is formed from cancer cells in vitro on Gelfoam®, but not on Matrigel™. J Cell Biochem 115:1362–1367

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert M. Hoffman .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Hoffman, R.M. (2018). 3D Sponge-Matrix Histoculture: An Overview. In: Hoffman, R. (eds) 3D Sponge-Matrix Histoculture. Methods in Molecular Biology, vol 1760. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7745-1_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-7745-1_2

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-7743-7

  • Online ISBN: 978-1-4939-7745-1

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics