Soil Binds Prions and Influences Their Biologic Properties - ACS

Chapter 20

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Soil Binds Prions and Influences Their Biologic Properties S. L. Bartelt-Hunt,*,1 S. E. Saunders,2 and J. C. Bartz3 1Department

of Civil Engineering, University of Nebraska-Lincoln, 203B Peter Kiewit Institute, Omaha, Nebraska 68182-0178 2Stanford University Law School, 559 Nathan Abbott Way, Stanford, California 94305-8610 3Department of Medical Microbiology and Immunology, Creighton University, 2500 California Plaza, Omaha, Nebraska 68178 *E-mail: [email protected]

The prion protein is believed to be the causative agent of a host of fatal neurodegenerative diseases, including chronic wasting disease and scrapie. The prion protein is shed into the environment and is strongly bound to soil. Evidence suggests that binding to soil can influence the biologic properties of the prion protein, including prion replication and infectivity. The physicochemical properties of soil influence this behavior, and some evidence suggests that local soil type may play a role in prion disease transmission in the environment.

The Prion Protein Prion Diseases Prion diseases, also called transmissible spongiform encephalopathies (TSEs), are a group of inevitably fatal neurodegenerative diseases that impact a number of mammalian species and include bovine spongiform encephalopathy (‘mad cow’ disease), scrapie, chronic wasting disease, transmissible mink encephalopathy, and Creutzfeldt-Jakob disease (1). Clinical symptoms of prion diseases include dementia, impaired motor control, and irregular behavior (2, 3). Prion diseases are distinguished pathologically by spongiform degeneration of the brain and accumulation of the abnormal prion protein in the central nervous system (1). © 2012 American Chemical Society In Proteins at Interfaces III State of the Art 2012; Horbett, T., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2012.


Strong evidence indicates that the infectious agent of TSEs (i.e. the prion, PrPSc) is an abnormally-folded conformer of a normal cellular protein, PrPc (4–6). The folded conformation of PrPSc conveys distinct biological and physicochemical properties to PrPSc, including resistance to proteolysis, increased hydrophobicity (and thus, decreased solubility in aqueous solvents), and a propensity for aggregation (1). The normal prion protein is a cell surface glycoprotein that has been identified in numerous mammalian species and is expressed most abundantly in the central nervous system but also in lymphoid cells, lung, heart, gastrointestinal tract, muscle, and other locations throughout the body (7). The function of the normal form of the prion protein has not been determined, but experiments suggest that it is involved in protection of the cell from oxidative damage (8). It is known that PrPc binds strongly with copper and other trace metals, and its function may therefore involve interactions with these metals in vivo (9). The conversion of PrPc to the PrPSc conformation is the central event in prion agent replication. The amino acid sequence of PrPc and PrPSc is the same, and thus the only identified difference is protein conformation (10). PrPSc has a higher β-sheet content and a decreased α-helix content compared to PrPc (11).

Figure 1. Elk PrPc nuclear magnetic resonance-derived structure. Image from The Worldwide Protein Bank (www.wwpdb.org). Adapted from ref. (12).

The tertiary structure of PrPc has been determined by nuclear magnetic resonance (NMR) and other methods (12), but that of PrPSc is still unknown due to the insolubility of its aggregates. Figure 1 shows an NMR-derived image of the structure of elk PrPc. PrPc consists of a flexibly disordered N-terminal tail, a well structured globular domain, and a flexibly disordered C-terminal (12). A disulfide bond joins two cysteines in the C-terminal region (9). PrPc is thought to exist mostly as a soluble monomer. A trimeric model has been proposed for PrPSc, where trimers of PrPSc combine to form the characteristic fibrils that accumulate in the central nervous system of diseased animals (9). PrPSc is very resistant to protease degradation; however, the N-terminal domain of PrPSc is vulnerable to degradation possibly because it is on the exterior of the structure. PrPSc resistance 434 In Proteins at Interfaces III State of the Art 2012; Horbett, T., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2012.

to proteases is often used to distinguish PrPSc from PrPc. For example, proteinase K (PK) completely degrades PrPc with incubation at 37°C for short periods (50 pH 7

4 h

purified HY (hamster) PrPSc

(35)

Fine quartz sand

0.0001

1h-60 days

HY (hamster) BH

(40)

Quartz microparticles

13.6-27.1

2 h


(34)

Mica

ND

1 h

ovine recPrP

(38)

Kaolinite

1.7-2.6

2 h


(34)

≈50

10 min

murine recPrP

(36)

Continued on next page.

441 In Proteins at Interfaces III State of the Art 2012; Horbett, T., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2012.

Table 2. (Continued). Review of prion sorption literature Sorption Capacity (µgPrP/mg)

Equilibration Time

Prion Material Used

Reference

ND

10 h

ovine recPrP

(46)

87-174

2 h


(34)

1000

2 h

ovine recPrP, C-term recPrP

(34)

>1200

10 min

murine recPrP

(36)

Montmorillonite- Ca2+

>400

10 min

murine recPrP

(36)

Bentonite- Na+

0.04

1h-20 d

HY (hamster) BH

(40)

Soil/Mineral


Montmorillonite- Na+

Abbreviations - ND: not determined, OM: organic matter, BH: brain homogenate.

Influence of Prion Strain, Species, and N-terminal Truncation on Prion Adsorption to Soil The environmental fate of PrPSc may vary with strain and species. Prion strains are operationally defined by distinct neuropathological characteristics (52). The amino acid sequence of PrP is species specific, and PrPSc conformation is strain dependent (53–57). A quantitative comparison of prion adsorption to soil as a function of prion strain and species was conducted by Saunders et al. (58). It was determined that the competitive matrix in which prions enter the environment can significantly affect prion interactions with soil, and that these interactions will vary with prion strain and species. In these experiments, brain tissue from hamsters infected with the HY TME and DY TME (drowsy strain of TME) agents at terminal disease as well as brain tissue from uninfected hamsters and an elk infected with CWD were used. Sorbents investigated included fine sand, sandy loam soil, and silty clay loam soil (Table 1). For batch isotherm studies, brain homogenate was combined with each sorbent for a total volume of 200 µl in DPBS in 0.2ml PCR tubes at pH 7. Mass ratios of total brain equivalents (BE) to soil ranged from 1:0.05 to 1:20. The soil-brain homogenate mixtures were incubated at 22°C and rotated at 24 rpm. Samples were removed at specified time points and allowed to settle or centrifuged at 100 g for 5 sec. For isotherm experiments, samples were equilibrated for 1 week (168 hr) unless otherwise noted. The supernatant was removed and the pellets were washed 2 times with DPBS. The original supernatant, first wash, and final pellet were collected and stored at -80°C. PrP in aqueous controls and samples was evaluated using a 96-well immunoblot assay (41) as described above in the section on prion kinetics. Prior to analysis, some samples were treated with proteinase K (PK) to quantify PrPSc sorption to soils. 442 In Proteins at Interfaces III State of the Art 2012; Horbett, T., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2012.


Maximum adsorption of HY TME PrP occurred at an intermediate aqueous concentration for sand and both whole soils (Figure 4A, C, and D). DY TME PrP adsorption was consistently lower than HY PrP for all sorbents, with similar isotherm shapes for DY and HY PrP. DY PrP adsorption was on average 60%, 65%, and 90% lower than HY for sand, sandy loam, and silty clay loam soils, respectively. In contrast to HY and DY PrP, CWD-elk PrP adsorption was maximal at the lowest concentration tested and decreased gradually as the aqueous concentration (Cw) increased (Figure 4B). Since the conformational differences between HY and DY PrPSc are not fully defined, it is difficult to explain the stronger adsorption affinity of HY PrP. Differences in PrPSc aggregation may be responsible. DY PrPSc is known to be more soluble than HY PrPSc in the presence of detergents (53), which may indicate it is less hydrophobic. Fundamental information on PrPSc structure and strain variance is needed before differences in adsorption can be explained.

Figure 4. Quantified isothermal studies of PrP adsorption. Panel A: HY TME PK-digested (HY PK+) or undigested (HY PK-), and DY TME undigested (DY PK-) PrP adsorption to fine quartz sand. Panel B: CWD-elk and uninfected (hamster) PrP adsorption to sand reported as normalized intensities. HY results are from Panel A. Panel C: Adsorption of HY PK+, HY PK-, and DY PK- PrP to sandy loam soil. Panel D: Adsorption of HY PK+, HY PK-, and DY PK- PrP to silty clay loam. Error bars show ± the standard error. N ≥ 3 for all points except 50 µg BE/µL points in A, B, & C and 100 µg BE/µL in D, where n = 1. Reproduced with permission from reference (58). Copyright 2009 American Chemical Society. 443 In Proteins at Interfaces III State of the Art 2012; Horbett, T., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2012.


Additional isotherms were generated using PK-digested HY TME brain homogenate. The N-domain of PrPSc is removed by proteinase K digestion, which also completely degrades PrPc (44). Isotherm shapes for PK-digested samples were similar to that observed for undigested samples (Figure 4). We have demonstrated previously that a large population of PrP will enter and exist in the environment without the N-terminal domain (44). Because the N-terminal domain is known to be flexibly-disordered and contains a high number of positively-charged amino acids, it may play a significant role in electrostatic attraction to negatively-charged mineral surfaces (46). Evidence suggests the N-domain might play a role in sorption to clays (29). However, the present results confirm previous reports that the N-domain is not needed for prion adsorption (29, 34). PK-digested PrPSc adsorption to sand and sandy loam soil was on average 8-fold and 2-fold greater, respectively, than PrP in undigested homogenate (Figure 4A and 4C). In contrast, PrPSc adsorption (PK+) to silty clay loam soil was on average 50% less than undigested PrP (Figure 4D). This result is in agreement with a previous observation that more full-length recPrP adsorbs to montmorillonite clay than N-terminally truncated recPrP (27). The underlying reasons for the increased adsorption of PK-treated PrPSc to sand and sandy soils is not clear. The N-domain of PrPSc is susceptible to proteases and therefore is likely on the exterior of the molecule (44). Removal of the N-domain may eliminate steric hindrances, allowing PrPSc to adsorb more readily to quartz surfaces. PK-digestion may modify PrPSc aggregation, yielding a conformation that promotes interaction with quartz surfaces but is less preferential for clay surfaces. PrPSc aggregation may be an important factor in adsorption. In contrast to infectious tissue isotherms, PrPc (not aggregated) in uninfected hamster brain homogenate did not exhibit a distinct intermediate maximum (Figure 4B). Furthermore, accelerated fibrillation of a prion peptide on a silicon surface has been reported compared with peptide fibrillation in solution (59), and aggregation of other proteins upon adsorption has also been shown (60, 61). The results presented here provide further evidence that rodent models may not recapitulate the behavior of natural prion diseases, such as CWD,in the environment. In kinetic studies conducted with sand and sandy loam soil, HY PrP adsorption plateaued after 30 d, while CWD PrP adsorption continued to increase through at least 60 d (58). Furthermore, unlike HY and DY PrP, adsorption of CWD PrP did not exhibit an intermediate maximum after a 1 week equilibration time in isothermal experiments (Figure 4B). Strain differences in PrP adsorption were also observed as HY TME PrP consistently exhibited greater sorbed phase concentrations than DY TME PrP. HY and DY are both hamster strains and therefore exist in similar brain homogenate matrices but differ in the three-dimensional structure of PrPSc (53–55, 57). It is possible that equal amounts of DY and HY PrP adsorb, but that the resulting conformation or orientation of bound DY PrP yields a decreased affinity for the primary antibody (mAb 3F4) compared with bound HY PrP. This would imply different adsorption mechanisms between the two strains.



Changes in the brain homogenate matrix due to PK-digestion may be partially responsible for differences in truncated and full-length PrPSc adsorption. A coomassie blue stain comparing the total protein before and after PK-digestion indicated a 60% decrease in protein content upon digestion, with a majority of the remaining peptides less than 14kDa (Figure 5). Thus, PK-digested homogenate has fewer large polypeptides than undigested homogenate to compete for adsorption sites, possibly allowing more PrPSc to adsorb. In addition, PK-digestion may reduce constituents which favorably or unfavorably coat or modify soil surfaces.

Figure 5. Total protein degradation due to PK digestion. On the left: representative Coomassie Blue stain of 2.5 µl of 10% HY TME- infected BH treated or untreated with proteinase K. M: molecular weight marker. On the right: signal intensities of digested samples (n = 4) were normalized against un-digested samples (n = 5). Error bars show ± 1 standard error of the mean. Reproduced with permission from reference (58). Copyright 2009 American Chemical Society.

Influence of Soil Binding on the Biologic Properties of the Prion Protein Information regarding the ability of soil-bound prions to replicate (i.e. convert PrPc to PrPSc) and initiate infection in a host animal is important for understanding environmental CWD and scrapie transmission. It has been demonstrated that HY TME (hamster) PrPSc bound to montmorillonite clay and three whole soils remains infectious via oral inoculation (62). In a previous study, we utilized protein misfolding serial amplification (PMCA) and animal bioassay to quantitatively compare unbound and soil-bound prion replication and infectivity to further investigate the influence of soil binding on the biologic properties of the prion protein. 445 In Proteins at Interfaces III State of the Art 2012; Horbett, T., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2012.


Figure 6. Single-round semi-quantitative PMCA. (A): Representative blots of serial dilutions of a HY TME brain homogenate subjected to one round of PMCA, shown with a 200 µg BH control. All samples PK-digested and blotted with mAb 3F4. For reference, the frozen (PMCA–) signal of the 10-2 dilution (not shown) is at the limit of western blot detection. (B): Quantification of blots shown in (A). Amplified signal was calculated by normalizing blot intensities (n ≥ 3) to 200 µg HY TME controls (n = 4) run on the same gel and then normalized to 10-1 HY controls subjected to PMCA concurrently. Error bars show ±1 standard error of the mean. Reproduced with permission from reference (30). Copyright 2011 American Society for Microbiology.

Protein misfolding cyclic amplification (PMCA) is a method developed by Claudio Soto and colleagues (63, 64) for studying prion replication (i.e. conversion of PrPc to PrPSc). It has been used to study the basic components of the infectious prion agent (65, 66), for detection of low levels of prions (67–69), and to investigate prion strain propagation (70–73). The PMCA method is somewhat analogous to polymerase chain reaction (PCR). It consists of cycles of sonication followed by incubation at 37°C. In this manner very small amounts of PrPSc can be amplified and detected by normal western blotting. An infectious seed (whether brain homogenate, soil, or other material) is added to uninfectious brain homogenized in a ‘conversion buffer’. The sample is then subjected to repeated cycles of sonication followed by incubation at 37°C. An unsonicated/unincubated control is kept frozen for comparison. After a specified number of cycles (designated as one PMCA round), the samples are diluted in fresh uninfected brain homogenate and then subjected to more cycles of sonication and incubation. PrPSc is then assayed for in samples and controls using western blot. It is hypothesized that the PMCA method works by breaking PrPSc aggregates with sonication, then allowing these smaller fragments to recruit and convert PrPc in the uninfectious brain homogenate substrate, generating more PrPSc. Newly generated PrPSc from PMCA has been shown to be infectious (73). A relationship exists between the input titer of prions and the number of serial PMCA rounds required for PrPSc detection (73, 74). A serial dilution of HY TME brain homogenate (with initial titer of 109.3 intracerebral (i.c.) 50% Lethal Dose (LD50) per gram) was performed in triplicate, and the amplified signal of 446 In Proteins at Interfaces III State of the Art 2012; Horbett, T., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2012.

each sample after a single round of PMCA was evaluated (Figure 6). PMCA generated PrPSc was detected in all samples down to an input dilution of 10-4.3 µg equivalents (103.0 i.c. LD50) of brain homogenate (Figure 6A). A logarithmic relationship (R2 =0.97) best approximated the association between the input titer of HY TME agent and the abundance of PMCA generated PrPSc (Figure 6B).


Adsorption of PrPSc to Soil Reduces Prion Replication in Vitro Saunders et al. (30) determined that adsorption of HY TME and CWD PrPSc to soil reduces prion replication via PMCA. Both unbound and soil-bound HY TME was subjected to PMCA (Figure 7A), and compared to the unbound sample, sorption of HY TME to a silty clay loam soil (Table 1) resulted in a 92% reduction in the abundance of amplified PrPSc (Figure 7A, lanes 5 and 9). An unbound HY control co-spiked with SCL soil (Figure 7A, lanes 6 and 7) was less amplified than the unbound HY control but significantly (p0.05) suggesting that SCL binding to HY PrPSc does not permanently alter the agent. All diseased animals exhibited clinical signs of hyperexcitability and ataxia and PrPSc migration properties that were consistent with HY TME agent infected animals.


Table 3. Reduced titer of soil-bound HY TME agent. Reproduced with permission from reference (30). Copyright 2011 American Society for Microbiology Inoculum


Agent dilution

a

HY TME

HY TME sorbed to SCL

10-2

62±3 (5/5)a

74±3 (5/5)

10-3

n.d.

78±3 (5/5)

10-4

74±4 (5/5)

84±3 (5/5)

10-5

n.d.

96±3 (5/5)

10-6

98±3 (5/5)

120±25 (3/5)

10-7

127±18 (5/5)

>275 (0/5)

10-8

>275 (0/5)

>275 (0/5)

10-9

>275 (0/5)

>275 (0/5)

Mock

>275 (0/5)

>275 (0/5)

Titer:

107.5

106.2 i.c. LD50/25µl

i.c. LD50/25µl

Mean incubation period in days±SEM (number affected/number inoculated).

Do Soil Properties Influence Prion Disease Incidence? As CWD in particular continues to spread geographically and disease residence times in cervid populations and habitats increases, environmental factors may play an increasingly important role in sustaining or heightening disease prevalence (76). It is possible that the residence time of prions in the environment as well as the efficiency of prion transmission could vary significantly with local soil properties. Experimental data on the influence of prion-soil interactions on the biologic properties of the protein outlined above clearly provide the basis for potential variance in prion incidence due to soil factors, most especially soil type. The influence of soil factors on disease incidence is certainly not without precedent, however, the epidemiological data on prion soil risk factors are as yet limited (77, 78).

Acknowledgments This work was supported by National Science Foundation (CBET-1149242) and the Nation Center for Research Resources (P20 RR0115635-6, C06 RR1741701 and G200RR024001).


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