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Interaction between bacteria and the lumenal bladder surface: modulation by pentosan polysulfate, an experimental and theoretical approach with clinical implication

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An attempt was made to interpret bacterial adsorption to the lumenal surface of the urinary bladder wall under normal and pathological conditions according to the DLVO theory of lyophobic colloid stability, which describes the interaction between a bacterium and the bladder-wall surfaces as a balance of attraction and repulsion forces. Computer modeling suggested that a decrease in the surface potential of the bladder wall may well explain an increased bacterial adsorption, possibly associated with bacterial cystitis. With the intent of preventing bacterial adsorption, treatment of bacterial cystitis by intravesical instillation of pentosan polysulfate (PPS) was evaluated. PPS is a polysaccharide with high affinity (4±2 mg/bladder) to the bladder. The attachment of PPS strongly depends on the intrinsic properties of the bacterial surface. Theoretical considerations indicate that either complete coverage of the bacterium with PPS or an absence of PPS affinity is a prerequisite for obtaining steric interaction or prevention of bacterial sorption. Experimentally, an absence of PPS affinity (0–0.7 μg/mg bacteria) was found for bacteria commonly found during cystitis. Immunological treatment of superficial bladder cancer by bacillus Calmette-Guérin (BCG) depends on the interaction of BCG with the bladder wall. Improvement of the treatment may be obtained by increasing BCG adsorption. In this respect, the phenomenon of bridging in which PPS binds simultaneously to both BCG and the bladder-wall surface was investigated. Theoretical considerations and experimental results appeared to be in good agreement. It was found that BCG binds a considerable amount of PPS (3.4±0.3 μg/mg BCG). In a guinea pig model the theoretical considerations, indicating the occurrence of bridging at a low and narrow range of PPS concentrations, seemed to be confirmed. In contrast to a high PPS concentration of 10 mg/ml, at a low (0.1 mg/ml) PPS concentration a significant stimulation of the BCG-associated immune reaction(s) was observed. The results suggest that to obtain PPS-induced bridging between BCG and the bladder wall and to prevent steric interaction, PPS should be instilled prior to BCG, separated by extensive washout of free PPS.

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References

  1. Bangham AD, Pethica BA (1960) The adhesiveness of cells and the nature of chemical groups at their surfaces. Proc R Phys Soc (Edinburgh) 28:43–52

    Google Scholar 

  2. Böhle A, Nowc CH, Ulmer AJ, Musehold J, Hofstetter AG, Flad H-D (1992) Elevations of cytokines interleukin-1, interleukin-2 and tumor necrosis factor in the urine of patients after intravesical bacillus Calmette-Guérin immunotherapy. J Urol 144:59–64

    Google Scholar 

  3. De Boer EC, Jong WH de, Steerenberg PA, Aarden LA, Tetteroo E, Groot ER de, Meijden APM van der, Vegt PDJ, Debruyne FMJ, Ruitenberg EJ (1992) Induction of urinary IL1, IL2, IL6, and TNF during intravesical immunotherapy with BCG in superficial bladder cancer. Cancer Immunol Immunother 34:306–312

    Google Scholar 

  4. De Boer EC, Jong WH de, Meijden APM van der, Steerenberg PA, Witjes JA, Vegt PDJ, Debruyne FMJ, Ruitenberg EJ (1991) Presence of activated lymphocytes in the urine of patients with superficial bladder cancer after intravesical immunotherapy with bacillus Calmette-Guérin. Cancer Immunol Immunother 33:411–416

    Google Scholar 

  5. De Boer EC, Steerenberg PA, Meijden APM van der, Klingeren B van, Jong WH de, Debruyne FMJ, Ruitenberg EJ (1992) Impaired immune response by isoniazid treatment during intravesical BCG administration in the guinea pig. Prog Clin Biol Res 378:81–93

    Google Scholar 

  6. De Reijke TM, Boer LC de, Steerenberg PA, Vos PCN, Kurth KH, Schamhart DHJ (in press) The effects of intravesical pretreatment with pentosanpolysulfate on the bacillus Calmette-Guérin induced immune reaction of the guinea pig. J Urol

  7. De Reijke TM, Vos PCN, Boer EC de, Bevers RFM, Muinck Keizer WH de, Kurth KH, Schamhart DHJ (in press) Cytokine production by the human bladder carcinoma cell line T24 in the presence of bacillus Calmette-Guérin (BCG). Urol Res 21

  8. Derjaguin VB, Landau LD (1941) Acta Phys Chim USSR 14:633

    Google Scholar 

  9. Falkow S (1991) Bacterial entry into eukaryotic cells. Cell 65:1099–1102

    Google Scholar 

  10. Finlay BB, Falkow S (1989) Common themes in microbial pathogenicity. Microbiol Rev 53:210–230

    CAS  PubMed  Google Scholar 

  11. Garden RJ, Liu BC-S, Redwood SM, Weiss RE, Droller MJ (1992) Bacillus Calmette-Guérin abbrogates in vitro invasion and motility of human bladder tumor cells via fibronectin interaction. J Urol 148:900–905

    Google Scholar 

  12. Haydon DA (1961) The surface charge of cells and some other small particles as indicated by electrophoresis. I. The zeta potential-surface charge relationships. Biochim Biophys Acta 50:450–457

    Google Scholar 

  13. Haydon DA (1961) The surface charge of cells and some other small particles as indicated by electrophoresis. II. The interpretation of the electrophoretic charge. Biochim Biophys Acta 50:457–462

    Google Scholar 

  14. Herr HW, Laudone VP, Whitmore WF Jr (1987) An overview of intravesical therapy for superficial bladder tumors. J Urol 138:1363–1368

    Google Scholar 

  15. Holm-Bentzen M, Jacobsen F, Nerstrom B, Lose G, Kristensen JK, Pedersen RH, Krarup T, Feggetter J, Bates P, Barnard R, Larsen S, Hald T (1987) A prospective double-blind clinically controlled multicenter trial of sodium pentosulfate in the treatment of interstitial cystitis and related painful bladder disease. J Urol 138:503–507

    Google Scholar 

  16. Hurst RE, Rhodes SW, Adamson PB, Parsons CL, Roy JB (1987) Functional and structural characteristics of the glycosaminoglycans of the bladder luminal surface. J Urol 138:433–437

    Google Scholar 

  17. Isberg RR (1991) Discrimination between intracellular uptake and surface adhesion of bacterial pathogens. Science 252:934–938

    Google Scholar 

  18. Isberg RR Leong JM (1990) Multiple β1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60:861–871

    Google Scholar 

  19. Kalager T, Andersen BM, Bergan T, Brubakk O, Bruun JN, Doskeland B, Hellum KB, Hopen G, Lippe E von der, Rahm VR, Ritland S, Schreiner A (1992) Ciprofloxacin versus a tobramycin/cefuroxime combination in the treatment of serious systemic infections: a prospective, randomized and controlled study of efficacy and safety. Scand J Infect Dis 24:637–646

    Google Scholar 

  20. Kavoussi LR, Brown EJ, Ritchey JK, Ratliff TL (1990) Fibronectin-mediated Calmette-Guérin bacillus attachment to murine bladder mucosa. J Clin Invest 85:62–67

    Google Scholar 

  21. Marshall KC (1980) Bacterial adhesion in natural environments. In: Berkeley RCW, Lynch JM, Melling J, Rutter PR, Vincent B (eds) Microbial adhesion to surfaces. Ellis Horwood, Chichester, pp 187–196

    Google Scholar 

  22. Marshall KC, Stout R, Mitchell R (1971) Mechanisms of the initial events in the sorptin of marine bacteria to surfaces. J Gen Microbiol 68:337–348

    Google Scholar 

  23. McKeown-Longo PJ (1987) Fibronectin-cell surface interactions. Rev Infect Dis 9:S322-S334

    Google Scholar 

  24. Napper DH (1977) Steric stabilisation. J Colloid Interface Sci 58:390–407

    Google Scholar 

  25. Nir S (1977) Van der Waals forces between surfaces of biological interest. Prog Surface Sci 8:1–58

    Google Scholar 

  26. Olsson J, Glantz PO, Krasse B (1976) Surface potentials and adherence of oral streptococci to solid surfaces. Scand J Dental Res 84:240–242

    Google Scholar 

  27. Pantazopoulos D, Legakis N, Antonakopoulos G, Sofras F, Dimopoulos C (1987) The effect of pentosanpolysulfate and carbenoxolone on bacterial adherence to the injured urothelium. Br J Urol 59:423–426

    Google Scholar 

  28. Parsons CL (1982) Prevention of urinary tract infection by the exogenous glycosaminoglycan sodium pentosanpolysulfate. J Urol 127:167–169

    Google Scholar 

  29. Parsons CL, Boychuk D, Jones S, Hurst R, Callahan H (1990) Bladder surface glycosaminoglycans: an epithelial permeability barrier. J Urol 143:139–142

    Google Scholar 

  30. Parsons CL, Mulholland SG (1987) Successful therapy of interstitial cystitis with pentosan polysulfate. J Urol 138:513–515

    Google Scholar 

  31. Parsons CL, Pollen JJ, Anwar H, Stauffer C, Schmidt JD (1980) Antibacterial activity of bladder surface mucin duplicated in the rabbit bladder by exogenous glycosaminoglycan (sodium pentosanpolysulfate). Infect Immun 27:876–881

    Google Scholar 

  32. Parsons CL, Stauffer C, Schmidt JD (1980) Bladder surface glycosaminoglycans: an efficient mechanism of environmental adaptation. Science 208:605–607

    Google Scholar 

  33. Pethica BA (1961) The physical chemistry of cell adhesion. Exp Cell Res 8 [Suppl]: 123–140

    Google Scholar 

  34. Pethica BA (1980) Microbial and cell adhesion. In: Berkeley RCW, Lynch JM, Melling J, Rutter PR, Vincent B (eds) Microbial adhesion to surfaces. Ellis Horwood, Chichester, pp 19–45

    Google Scholar 

  35. Pollack W, Hager HJ, Reckel R, Toren DA, Singher HO (1965) A study of the forces involved in the second stage of haemagglutination. Transfusion 5:158–183

    Google Scholar 

  36. Ratliff TL (1992) Mechanisms of action of BCG in superficial bladder cancer. Prog Clin Biol Res 378:103–109

    Google Scholar 

  37. Reitsma DJ, Guinan P, Lamm DL, Khanna OP, Brosma SA, DeKernion JB, Williams RD, Simpson G, Hanna MG Jr (1989) Long-term effect of intravesical bacillus Calmette-Guérin (BCG) Tice strain on flat carcinoma in situ of the bladder. Prog Clin Biol Res 310:171–185

    Google Scholar 

  38. Ruoslahti E (1991) Integrins. J Clin Invest 87:1–5

    Google Scholar 

  39. Rutter PR, Vincent B (1980) The adhesion of micro-organisms to surfaces: physico-chemical aspects. In: Berkeley RCW, Lynch JM, Melling J, Rutter PR, Vincent B (eds) Microbial adhesion to surfaces. Ellis Horwood, Chichester, pp 79–92

    Google Scholar 

  40. Schamhart DHJ, Boer LC de, Bevers RFM, Kurth KH, Steerenberg PA (1992) Mycobacterial adherence and BCG treatment of superficial bladder cancer. Prog Clin Biol Res 378:75–89

    Google Scholar 

  41. Schamhart DHJ, Kurth KH (1993) Aspekte der Reaktion von Harnblasenkarzinomzellen und der Harnblase von Patienten mit oberflächlichem Harnblasenkarzinom auf BCG. In: Rübben H, Goepel M, Schmitz-Dräger BJ (Hrsg) Immuntherapie in ter Uroonkologie. Springer, Berlin Heidelberg New York, S199–207

    Google Scholar 

  42. Schamhart DHJ, Kurth KH, Reijke TM de, Vleeming R (1992) BCG treatment and the importance of an inflammatory response. Urol Res 20:199–209

    Google Scholar 

  43. Scurr DS, Robertson WG (1985) Studies on the mode of action of polyanionic inhibitors of calcium oxalate crystallization in urine. In: Schwille PO, Smith LH, Robertson WG, Vahlensieck W (eds) Urolithiasis and related clinical research. Plenum, New York, pp 835–838

    Google Scholar 

  44. Shaw DJ (1980) Introduction to colloid and surface chemistry. Butterworth, London

    Google Scholar 

  45. Tadros TF (1980) Particle-surface adhesion. In: Berkeley RCW, Lynch JM, Melling J, Rutter PR, Vincent B (eds) Microbial adhesion to surfaces. Ellis Horwood, Chichester, pp 94–116

    Google Scholar 

  46. Teppema JS, De Boer EC, Steerenberg PA, Meijden APM van der (1992) Morphological aspects of the interaction of bacillus Calmette-Guérin (BCG) with urothelial cells in vivo and in vitro: relevance for antitumor activity? J Urol 20:219–227

    Google Scholar 

  47. Meijden APM van der, Jong WH de, Boer EC de, Steerenberg PA, Debruyne FMJ, Ruitenberg EJ (1989) Immunological aspects of intravesical administration of bacillus Calmette-Guérin (BCG) in the guinea pig. Urol Res 17:47–55

    Google Scholar 

  48. Verwey EJW, Overbeek JThG (1948) Theory of stability of lyophobic colloids. Elsevier, Amsterdam

    Google Scholar 

  49. Vincent B (1974) The effect of adsorbed polymers on dispersion stability. Adv Colloid Interface Sci 4:193–277

    Google Scholar 

  50. Vincent B, Young CA, Tadros TFT (1978) Equilibrium aspects of heteroflocculation in mixed sterically stabilised dispersions. Faraday Discuss Chem Soc 65:296–305

    Google Scholar 

  51. Vincent B, Young CA, Tadros TFT (1980) Adsorption of small positive particles onto large negative particles in the presence of polymer. I. Adsorption isotherms. J Chem Soc Faraday Trans [I] 76:665–673

    Google Scholar 

  52. Weiss L (1968) Studies on cellular adhesion in tissue culture. IX. Electrophoretic mobility and contact phenomena. Exp Cell Res 51:609–625

    Google Scholar 

  53. Weiss L (1968) Studies on cellular adhesion in tissue culture. X. An experimental and theoretical approach to interaction forces between cells and glass. Exp Cell Res 53:603–614

    Google Scholar 

  54. Weiss L, Blumenson LE (1967) Dynamic adhesion and separation of cells in vitro. II. Interactions of cells with hydrophilic and hydrophobic surfaces. J Cell Physiol 70:23–32

    Google Scholar 

  55. Weiss L, Woodbridge RF (1967) Some biophysical aspects of cell contacts. Fed Proc 28:88–94

    Google Scholar 

  56. ZoBell CE (1943) The effect of solid surfaces upon bacterial activity. J Bacteriol 46:39–59

    Google Scholar 

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Authors and Affiliations

  1. Department of Urology, University of Amsterdam, Meibergdreef 9, NL-1105 AZ, Amsterdam, The Netherlands

    D. H. J. Schamhart, E. C. de Boer & K. H. Kurth

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  1. D. H. J. Schamhart
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  2. E. C. de Boer
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  3. K. H. Kurth
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Supported by a grant from the Urological Research Foundation Amsterdam (BUWO) and bene Arzneimittel, Germany.

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Schamhart, D.H.J., de Boer, E.C. & Kurth, K.H. Interaction between bacteria and the lumenal bladder surface: modulation by pentosan polysulfate, an experimental and theoretical approach with clinical implication. World J Urol 12, 27–37 (1994). https://doi.org/10.1007/BF00182048

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